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Effects of Land-Use Change on the Conservation of Bird Species in the

Path of the Tapir Biological Corridor, Costa Rica

A Dissertation

Presented to the Faculty of the Graduate School


of
Yale University
in Candidacy for the Degree of
Doctor of Philosophy

by

Alvaro Redondo Brenes

Dissertation Director: Dr. Florencia Montagnini and Dr. Chadwick Oliver

May 2010
Abstract

Effects of Land-Use Change on the Conservation of Bird Species in the Path of the
Tapir Biological Corridor, Costa Rica

By Alvaro Redondo-Brenes

2010

I studied bird species diversity within ten different land-use types in the human-

modified and fragmented Path of the Tapir Biological Corridor, Costa Rica. The ten land-

use types were wildlife refuges, biological reserves, tree plantations, forest fallows, forest

edges, villages, residential tourism projects, homegardens, agrosilvopastoral systems, and

oil palm plantations. I was interested in determining how important the ten different

habitat types are for maintaining the bird diversity of the corridor and how these land

uses can be managed to enhance their conservation value. To address these questions I

selected 20 different sampling points within each habitat type. Bird surveys were carried

out over a two-year period. Each point was surveyed three times over the dry and three

times over the rainy periods of each year, total 12 visits per point. Total observation time

for all surveys was 400 hours. Aside from bird identification, I also recorded bird

activities (e.g. foraging, nesting) and microhabitats where they were observed (e.g. tree,

shrub, ground).

I found a total of 44,917 birds from 48 families, and 334 species. Eighty one

percent of the birds were recorded utilizing forested habitats. However, 77% of the

registered birds were also found in the human-modified land-use types. Moreover,

44.5% of species were classified as forest specialist, 38.9% forest generalist, and 16.6%

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open area specialist. Regarding feeding guilds, 53.8% of species were classified as

insectivores, 21.2% frugivores, 9% nectarivores, and carnivores and granivores 8% each.

I also identified 32 threatened species and 22 endemic species. Eight of the 22 endemic

species were also under threat, and three endangered species were registered: Ara macao,

Amazilia boucardi, and Icterus mesomelas. Overall, 64% and 75% of endemic and

threatened species, respectively, were forest-dependent species. It is suggested managing

the landscape in three units (protected areas, integrated management areas, and tree

plantations) that allow habitat for most species while providing income to local people.

Payment for environmental services, ecotourism, reforestation, environmental education

programs, and private investment, among others, could provide the incentives and

infrastructure that local people need to practice the suggested management effectively.

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Effects of Land-Use Change on the Conservation of Bird Species in the Path of the
Tapir Biological Corridor, Costa Rica

A Dissertation

Presented to the Faculty of the Graduate School


of
Yale University
in Candidacy for the Degree of
Doctor of Philosophy

by
Alvaro Redondo Brenes

Dissertation Director: Dr. Florencia Montagnini and Dr. Chadwick Oliver

May 2010

iii
2010 © by Alvaro Redondo Brenes
All Rights Reserved

iv
Table of Contents

Abstract……………………………………………………………………………… i

Table and Figures……………………………………………………………………. vii

Dedication…………………………………………………………………………… ix

Acknowledgements………………………………………………………………….. x

Chapter 1: A Review of the Effects of Land-Use Change and Habitat


Fragmentation on Wildlife Species Conservation…………………………………... 1

Chapter 2: Physical, Political, and Socio-Economic Aspects of the Path of the Tapir
Biological Corridor ……………………...………………………………………….. 17

Chapter 3: Avian diversity of ten land-use types in a human-modified biological


corridor in Costa Rica……………………………………………………………….. 58
Abstract……………………………………………………………………………… 58
Introduction………………………………………………………………………….. 59
Methods……………………………………………………………………………… 61
Results……………………………………………………………………………….. 67
Discussion…………………………………………………………………………… 71
Conclusions………………………………………………………………………….. 82
References…………………………………………………………………………… 84
Tables and Figures…………………………………………………………………... 92

Chapter 4: Response of bird guilds to ten land-use types in a human-modified


biological corridor, Costa Rica…………………..………………………………….. 99
Abstract……………………………………………………………………………… 99
Introduction………………………………………………………………………….. 100
Methods……………………………………………………………………………… 102
Results……………………………………………………………………………….. 104
Discussion…………………………………………………………………………… 108
Conclusions………………………………………………………………………….. 116
References…………………………………………………………………………… 118
Tables and Figures…………………………………………………………………... 123

Chapter 5: Conservation of threatened and endemic bird species in a human-


modified biological corridor: sustainable forestry criteria recommendations............. 131
Abstract……………………………………………………………………………… 131
Introduction………………………………………………………………………….. 132
Methods……………………………………………………………………………… 134
Results……………………………………………………………………………….. 139
Discussion…………………………………………………………………………… 142
v
Conclusions………………………………………………………………………….. 158
References…………………………………………………………………………… 160
Tables and Figures…………………………………………………………………... 169

Summary and Conclusions………………………………………………………….. 177


APPENDIX 1: Abundance of 334 bird species found in the PTBC...………………. 183

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Tables and Figures

Chapter 2: Physical, Political, and Socio-Economic Aspects of the Path of the


Tapir Biological Corridor

Table 2.1 Summary of vegetation data for five land-use types in the Path of the
Tapir Biological Corridor, Costa Rica………………………………………………. 49
Table 2.2 Sorensen Similarity Index for woody species in four land-use types in the
Path of the Tapir Biological Corridor, Costa Rica………………………………….. 49

Figure 2.1 Location of the Path of the Tapir Biological Corridor, Costa Rica……… 50
Figure 2.2 Physical evidence of indigenous people settlements in the PTBC……… 51
Figure 2.3 Land-use change from 1992 to 2000 in the Path of the Tapir Biological
Corridor, Costa Rica. ………………………………………………………………. 52
Figure 2.4 Illegal logging and burning of mangrove forest found on a property in
Hatillo of Aguirre, Puntarenas, Costa Rica…………………………………………. 53
Figure 2.5 Political division of the Path of the Tapir Biological Corridor in three
Conservation Areas (ACOPAC, ACOSA, and ACLA-P) and four counties (Osa,
Aguirre, Perez Zeledon, and Dota)………………………………………………….. 54
Figure 2.6 Land-use types in the Path of the Tapir Biological Corridor in 2000,
Costa Rica…………………………………………………………………………… 55
Figure 2.7. Diameter size class distribution of tree species located in five land-use
types in the Path of the Tapir Biological Corridor, Costa Rica……………………... 56
Figure 2.8. Total height size class distribution of tree species located in five land-
use types in the Path of the Tapir Biological Corridor, Costa Rica…………………. 57

Chapter 3: Avian diversity of ten land-use types in a human-modified biological


corridor in Costa Rica

Table 3.1. Abundance, species richness, and diversity of birds registered in ten
land-use types in the Path of the Tapir Biological Corridor, Costa Rica…………… 92
Table 3.2. Sorensen similarity index and shared species of ten land-use types in the
Path of the Tapir Biological Corridor………………………………………………. 93

Figure 3.1. Location of the Path of the Tapir Biological Corridor, Costa Rica…….. 94
Figure 3.2 Accumulated number of bird species found in ten different habitat types
in the Path of the Tapir Biological Corridor, Costa Rica…………………………… 95
Figure 3.3. Relative abundance of the five more abundant bird families per land-
use type in the Path of the Tapir Biological Corridor, Costa Rica………………….. 96
Figure 3.4. Expected number of bird species in ten habitat types in the Path of the
Tapir Biological Corridor, Costa Rica……………………………………………… 97
Figure 3.5. Similarity of bird assemblages across ten habitat types in the Path of the
Tapir Biological Corridor, Costa Rica………………………………………….. 98

Chapter 4: Response of bird guilds to ten land-use types in a human-modified


biological, Costa Rica

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Table 4.1 Abundance and species richness per census (n=12) for habitat bird guilds
in 10 land-use types in the Path of the Tapir Biological Corridor, Costa Rica……... 123
Table 4.2 Abundance and species richness per census (n=12) for bird feeding
guilds located in 10 land-use types in the Path of the Tapir Biological Corridor,
Costa Rica…………………………………………………………………………… 124

Figure 4.1. Relative abundance of species by habitat guild (percentage of species) 125
within 10 land-use types in the Path of the Tapir Biological Corridor, Costa Rica…
Figure 4.2 Non-metric multidimensional scaling (NMDS) ordination of the
distribution of canopy forest specialist species in ten land-use types in the Path of
the Tapir Biological, Corridor ……………………………………………………… 126
Figure 4.3 Non-metric multidimensional scaling (NMDS) odination of the
distribution of understory forest specialist species in ten land-use types in the Path
of the Tapir Biological, Corridor ………………………………………………….. 127
Figure 4.4 Relative abundance of bird species by feeding guild (percentage of
species) within 10 land-use types in the Path of the Tapir Biological Corridor,
Costa Rica …………………………………………………………………………... 128
Figure 4.5 Relative abundance of birds (percentage of birds) for activity within 10
land-use types in the Path of the Tapir Biological Corridor, Costa Rica …………... 129
Figure 4.6 Relative abundance of birds by microhabitat (percentage of birds)
within 10 land-use types in the Path of the Tapir Biological Corridor, Costa Rica… 130

Chapter 5: Conservation of threatened and endemic bird species in a human-


modified biological corridor: sustainable forestry criteria recommendations

Table 5.1 Threatened and Endangered bird species found in the Path of the Tapir
Biological Corridor………………………………………………………………….. 169
Table 5.2 Endemic bird species found in the Path of the Tapir Biological Corridor.. 170

Figure 5.1 Abundance per census (N = 12) of endangered and threatened species 171
found in the Path of the Tapir Biological Corridor………………………………….
Figure 5.2 Abundance per census (N = 12) of endemic species found in the Path of
the Tapir Biological Corridor……………………………………………………….. 172
Figure 5.3. Relative abundance of endemic and threatened bird species by habitat
guilds found in the Path of the Tapir Biological Corridor, Costa Rica……………... 173
Figure 5.4 Relative abundance of endemic and threatened bird species by feeding
guilds found in the Path of the Tapir Biological Corridor, Costa Rica……………... 174
Figure 5.6. Non-Metric Multidimentional scaling (NMDS) ordination of threatened
and endangered species found in ten land-use types in the Path of the Tapir
Biological Corridor …………………………………………………………………. 175
Figure 5.7. Non-Metric Multidimentional scaling (NMDS) ordination for endemic
species found in ten land-use types in the Path of the Tapir Biological Corridor…... 176

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To my parents
Maria Eugenia and Alvaro Francisco,
who are always in my heart

ix
Acknowledgments

First of all, I would like to thank mentors, family, friends, and colleagues for their

support throughout my five years at the Yale School of Forestry and Environmental

Studies and at the Path of the Tapir Biological Corridor in Costa Rica.

My gratitude to Florencia Montagnini for the opportunity to work with her for the

last seven years, including two years as a Master of Forest Science Student. I am also

deeply grateful to my other committee members: Chad Oliver, Jonathan Reuning-Scherer

and David Skelly. Thank you all for sharing all your knowledge and for making my

dissertation thesis and time at Yale more meaningful and enjoyable.

My family and friends were always there, supporting me in the good and in the

bad moments. I am lucky to have you all. Without your support this dissertation would

not be possible.

In Costa Rica, especially in the Path of the Tapir Biological Corridor, I am

immensely thankful to all my collaborators and friends for helping me out with all the

data gathering and for the opportunity to learn new things every day I spent with you. All

your time and knowledge is invaluable. Thank you to Cristian Valenciano, my best friend

there, for the introduction to the Path of the Tapir in 2005. Thank you to ASANA, the

local NGO, and all its members, that collaborated throughout the dissertation process. I

also owe gratitude to Jack Ewing and Steve Stroud for allowing me to stay at Hacienda

Baru National Wildlife Refuge for more than two years. Thank you to all staff and friends

of ASANA and Hacienda Baru: Leti & family, Ronald, Pedro, Juan Ramon & family,

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Kika, Danny, Negro, Carlitos, Olman & family, Jose, Papo, among others I was lucky to

meet.

Aside from ASANA and Hacienda Baru, several families/organizations permitted

me to work on their properties and I am thankful to all of them. The Firestone Center for

Restoration Ecology (Pitzer College) not only provided me the opportunity to survey the

Finca Isla del Cielo, but also, Carol Brandt and Don McFarlane gave me the unique

opportunity to teach during my time in the corridor and use their facilities. Moreover,

Isabel, Greddy, Marianela, Francisco, students, and faculty were always supportive. I am

also indebted to the Odio Family (Rancho La Merced), the Duarte family (Oro Verde),

Geiner Guzman & family (La Cusinga), and all friends of La Guapil Reserve, for letting

me onto their properties. Pedro Porras was my mentor in bird identification, but also

Julian Odio, Danny and Janan Duarte, Juan Ramon, Noel Urena, and Cristian Valenciano

provided invaluable bird information for my dissertation.

Several governmental and non-governmental organizations also contributed to my

dissertation work such as INBio, MINAET, SINAC, MEP, ICE, AyA, ASADAS,

Municipalities, local organizations and of course local people.

This project was funded by the School of Forestry and Environmental Studies, the

Tropical Resources Institute, the Council for Latin American and Iberian Studies, the

Center for Field Biology Pilot Grant, and the John F. Enders Fellowships & Research

Grants, all of them at Yale University; and by the Evergreen Fellow Grant Program

through the NGO Friends of Osa and the Firestone Center for Restoration Ecology.

Thank you God for Costa Rica, for the Path of the Tapir, for Dominical and

surrounding areas. These areas and their people are unique.

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Chapter 1

A Review of the Effects of Land-Use Change and Habitat Fragmentation on Wildlife


Species Conservation

Introduction

The establishment of protected areas is one means of counteracting some of the

threats to biodiversity such as habitat loss and fragmentation (Sanchez-Azofeifa et al

2002; Polaski et al. 2005). As a result of this approach, in the last three decades there has

been an exponential growth in the number of protected areas worldwide, particularly in

tropical countries where biodiversity is greatest (Zimmerer et al. 2004; Naughton-Treves

et al. 2005). However, almost 90% of the world’s land surface still remains outside

formal protected areas (Dudley et al. 2005), particularly because of the socio-economic

and political constraints that limit the amount of land allocated to protected status.

Protected areas do not necessarily hold the extent of habitat needed by most living

species, forcing wildlife to seek habitat and refuge beyond the artificial boundaries of

these areas (Powell et al. 2000; Polaski et al. 2005; Dudley et al. 2005; Hilty 2006). In

fact, a recent study has shown that more than 12% of vertebrate species were not

represented in any protected area larger than 1,000 ha and in stricter conservation

classifications such as the IUCN Conservation categories (Rodrigues et al. 2004).

Costa Rica is not an exception, even though it is one of the most diverse countries

of the world (Obando 2002; 2007) and has one of the most significant systems of

protected areas (Groom et al. 2005), fragmentation and isolation of Costa Rican protected

areas are jeopardizing biological conservation (Powell et al. 2000; Sanchez-Azofeifa et

al. 2003). Given the limitations of the protected areas system in fragmented landscapes,

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several researchers have highlighted that a new conservation paradigm must incorporate

human-modified landscapes in assessments of biodiversity and ecosystem services,

planning of corridors, establishment of buffer zones, and restoration of degraded lands

(Chazdon et al. 2009).

This study was carried out in the fragmented and human-dominated Path of the

Tapir Biological Corridor (PTBC) in Costa Rica, which is one of the most diverse areas

of Central America (TNC-ASANA 2000), but whose biodiversity is at risk because of

deforestation and development. The PTBC’s main objective is to create a network of sites

favorable to fauna (e.g. tapirs) and flora between the forests of the Osa Peninsula and

Golfo Dulce and those located in the Los Santos Forest Reserve in the Talamanca

Mountain Range. The PTBC area covers approximately 82,000 ha, inhabited by

approximately 10,000 people in 55 rural communities.

The main goal of this study was to assess the contribution of ten different habitat

types to the conservation of bird species in the PTBC. The ten land-use types were:

biological reserves, wildlife refuges, homegardens, agrosilvopastoral systems, forest

edges, forest fallows, tree plantations, oil palm plantations, local villages, and residential

tourism projects.

Chapter (1) presents a theoretical background to understand the effects of

fragmentation, land-use change, and human-dominated landscapes on the conservation of

wildlife, focusing on tropical ecosystems and bird species. Chapter (2) presents a review

of physical and socio-economic characteristics of the PTBC: a description of the goals for

the creation the corridor as well as the ten different land-use types selected as part of the

dissertation goals, including vegetation types. Chapter (3) summarizes bird diversity in

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the PTBC, assessing differences in species composition across the ten land-use types.

Chapter (4) focuses on species composition in the ten land-use types based on bird habitat

and feeding guilds. Chapter (5) evaluates the potential contribution of these habitat types

to species of conservation concern (e.g endemic and threatened species). Furthermore,

based on the PTBC’s management goals, a set of sustainable forestry practices are

recommended.

Fragmentation and Land Use Change effects on wildlife species

Destruction or alteration of natural habitats by people because of land-use change,

represents one of the most serious threats to biodiversity worldwide (Groom et al. 2005),

along with climate change, nitrogen deposition, and invasive species (Sala et al. 2000).

As a consequence of this loss of natural habitats, there is the challenge of maintaining and

conserving biodiversity in fragmented landscapes now dominated by human land use

(Bennett 2003). Habitat fragmentation has two main components: (1) a reduction in the

area covered by a habitat type, or natural habitat generally, in a landscape; and (2) a

change in habitat configuration, with the remaining habitat left in smaller and more

isolated patches (Saunders et al. 1991). As a consequence of these changes at the

landscape level, Anderson and Jenkins (2006) suggested that habitat fragmentation may

lead to

(1) the elimination or dangerous reduction of populations of large, wide-ranging species,

including many top carnivores;

(2) the unraveling of entire biological communities – as, for example, when the decline of

top carnivores in fragmented habitats results in the “release” of smaller predators and

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herbivores, leading to overpredation or overgrazing that may eventually eliminate

species or destabilize communities;

(3) the destruction or degradation of remaining habitat through the intrusion of edge

effects such as altered microclimates or invasive species; and

(4) the disruption of key ecological processes dependent on increasingly rare animal

agents – such as pollination, seed dispersal, predator-prey interactions, and nutrient

cycling.

The response of wildlife species to habitat destruction and fragmentation is

influenced by the species’ home range area, body size, food resources and foraging

patterns, dispersal capabilities, nesting and shelter requirements, as well as tolerance to

habitat disturbance and sensitivity to altered microclimates (Bennett 2003). Based on

these animal characteristics, the species vulnerable to forest fragmentation can be

organized into six groups (Groom et al. 2005):

(1) Wide ranging species: Species such as large carnivores and migratory ungulates that

roam a large area in the course of their daily or seasonal movements. Also, animals of

heterogeneous landscapes such as amphibians and turtles are vulnerable to

fragmentation because they depend upon distinct habitats for different phases of their

life cycles.

(2) Non-flying species: Species with poor dispersal abilities may not travel far from

where they were born, or may be stopped by barriers such as a road or a clear-cut.

Examples are carrion beetles in Amazonian forests being fragmented by pasture

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development (Klein 1989), and arboreal mammals, peccaries, and many insect bats

that are unwilling to enter the matrix (Laurance et al. 2002).

(3) Species with specialized requirements: Species with specialized habitat or resource

requirements are often vulnerable to extinction, especially when those resources are

unpredictable in time or space. For example, the great green macaws (Ara ambigua)

nest and forage more than 90% of the time in almond trees (Dipteryx panamensis), so

the decrease of these trees has had a negative impact on the macaw population in

Costa Rica (Powell et al. 1999). Another example is the lotis blue butterfly

(Lycaeides argyrognomon lotis), an endemic species of California, USA that requires

open area. Because of suppression of natural fires in the 1970s, most grasslands

develop into dense forest, and the loss of habitat may have pushed it to extinction

(Oliver, C. pers. comm., January 2010).

(4) Large-Patch or Interior Species: Some species occur only in large patches of forests

or other habitats, and are absent from small patches with little or no true interior

habitat. For example, in Central Amazonia, many forest understory birds--including

army ant followers, solitary species, members of mixed-species flocks, and terrestrial

species--strongly avoid forest edges (Laurance 2004).

(5) Species with low fecundity: A species with low reproductive capacity cannot quickly

rebuild its population after a severe reduction caused by number of factors. For

example, large mammals such as the tapir and jaguar have low fecundity in

comparison with small mammals like rodents.

(6) Species vulnerable to human exploitation or persecution: Some species are actively

sought by people for food, furs, medicine, pets, or other uses; whereas other species,

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such as snakes and large predators, may be killed on sight. For example, as a result of

hunting, species such as the jaguar and peccaries have decreased populations in

Corcovado National Park in Costa Rica in the last two decades. The jaguar population

dwindled from 150 individuals in 1990 to only 30 individuals in 2004, and peccaries

from 2000 in 2000 to only 400 in 2004 (Carrillo 2004).

As a result of the concerns about the effects of habitat loss and fragmentation on

wildlife conservation, there have been an increasingly large number of studies on single

species or assemblages in fragmented landscapes throughout the world (Laurance and

Bierregaard 1997; see also a large list of papers summarized by Bennett 2003). However,

most of these studies have focused on the forest fragments themselves, ignoring species'

distribution in surrounding sites such as agricultural or other human-dominated areas

(Ricketts et al. 2000). Thus, there is a need to study the importance of the landscape

matrix for biological conservation.

Importance of the Landscape Matrix for Wildlife Conservation

Assessing the conservation potential of human-dominated landscapes requires

investigation of the activities, movement, and persistence of species not only in the

remnants of native habitats but also in the full array of countryside habitats surrounding

them (Sauders et al. 1991; Daily 2001; Hughes et al. 2002), known also as the matrix.

Lindenmayer and Franklin (2002) define matrix as the landscape areas that are not

designated primary for the conservation of natural ecosystems, ecological processes, and

biodiversity regardless of their current condition (i.e., whether natural or developed). The

matrix can also be defined as the most widespread habitat within which other elements

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are embedded, and it can be either the original habitat type (e.g., a primary forest now

surrounded by a matrix of agriculture) or a modified one (e.g., an agricultural plantation

surrounded by a matrix of pristine forest) (Anderson and Jenkins 2006). In

anthropogenically modified landscapes, some of the matrix or all of it may be human-

modified communities such as agricultural fields of various types, clear-cut forests,

pastures, tree plantations, fallow land, gardens, and towns (Daily et al. 2003; Hilty et al.

2006). In several tropical countries the spread of human-modified land-use types such as

croplands, pastures, and urban areas has been accompanied by biodiversity losses in the

last decades (Foley et al. 2005; Defries et al. 2010).

As part of the landscape, the matrix plays different roles for wildlife conservation:

(1) Matrix regulating the movement of organisms. The matrix has a significant effect

on connectivity in forest landscapes and in determining the quantity of successful

movements among habitat patches (Gascon et al. 1999; Lindenmayer and Franklin 2002;

Hilty et al. 2006), acting as a selective filter (not an absolute barrier) for the movement of

species across the landscape (Gascon et al. 1999). The type of vegetation cover in the

matrix determines the animal movement. What may facilitate the movement of one

species may be a barrier for other species (Anderson and Jenkins 2006). For example, a

matrix maintained in pasture may impede much faunal movement of forest-dependent

species (Gascon et al. 1999), but may facilitate open-area species movement (Sutcliffe

and Thomas 1996).

(2) Matrix as a resource. This is the case when the matrix can provide abundant food

resources that can be exploited by some species. In addition, the matrix may also offer

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access to some resources that are rarely needed by a species, perhaps seasonally, such as

forage plants rich in a scarce mineral, a favorable hibernation site, or access to a

pollinator (Hilty et al. 2006).

(3) Matrix as secondary habitat. It is possible that the matrix may serve as secondary

habitat for some populations (Lindenmayer and Franklin 2002; Hilty et al. 2006). This

situation is called a source-sink axis (Pulliam and Danielson 1991). The source

population is one in which reproduction is adequate to balance mortality and usually to

export surplus individuals, as well. Such a population supplies the residents with a

secondary habitat. Sink populations are those living in secondary habitat (Hilty et al.

2006). If sink populations produce enough offspring, those may supplement populations

in reserves (Lindenmayer and Franklin 2002; Hilty et al. 2006).

(4) Matrix as a sink or stopper. The matrix may function as a dispersal sink when the

matrix is large relative to the size of patches, when it does not support a resident

population of a target species, and when few other habitat patches are available to

dispersers (Hilty et al. 2006). In addition, the matrix may act as a “stopper” when it is a

complete barrier to dispersal (Hilty et al. 2006).

Several studies addressing the effect of the landscape matrix on wildlife

conservation have been conducted in the tropics (Gascon et al. 1999; Ricketts et al. 2000;

Hughes et al. 2002; Daily et al. 2003; Horner-Devine et al. 2003; Pereira et al. 2004).

Even though the authors mentioned above assert that there is no substitute for native

habitat, they also highlight the importance of human-dominated landscapes (e.g., coffee

plantations, pastures, tree plantations, secondary forests) for the conservation of

butterflies (Horner-Devine et al. 2003), non-flying mammals (Gascon et al. 1999; Daily

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et al. 2003), frogs (Gascon et al. 1999), moths (Ricketts et al. 2000), and birds (Lawton et

al. 1998; Gascon et al. 1999; Hughes et al. 2002; Lindell et al. 2004). For instance, in a

study of non-flying mammal species in the montane areas of Costa Rica, Daily et al.

(2003) found a total of 26 native species. From these 26 species, 9 (35%) were restricted

to forest habitat, 14 (54%) occurred in both forest and agricultural habitats, and 3 (11%)

were found only in agricultural habitats, showing that the majority of native mammals

use countryside habitats.

In the same region, Hughes et al. (2002) found a total of 144 bird species. For this

study it was estimated that 46% of those native to the region were utilizing the matrix in

some manner. Moreover, it was predicted that bird richness in the matrix would decline

to approximately 40% if tall trees and edge habitats were removed from the landscape.

Results of the Biological Dynamics of Forest Fragments Project (BDFFP) in central

Brazil also present differences in the behavior of wildlife in forest fragments and the

surrounding matrix (Gascon et al. 1999). Overall, for ants, small mammals, birds, and

frogs, it was found that between 8-15% of the nominally primary-forest species were

recorded in matrix habitats. In addition, the three vertebrate groups (mammals, frogs, and

birds) exhibited positive and significant correlations between matrix abundance and

vulnerability to fragmentation, suggesting that species that avoid the matrix tend to

decline or disappear in fragments, while those that tolerate or exploit the matrix often

remain stable or increase (Gascon et al. 1999).

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Enhancing wildlife conservation through biological corridors

Minimizing the effects of isolation by enhancing landscape connectivity is one

way to counter the adverse effects of fragmentation (Noss 1987; Bennett 2003), in

addition to increasing the effective habitat area (Noss 1987). Connectivity can be defined

as linkages of habitats, communities, and ecological processes at multiple spatial and

temporal scales (Noss 1991). Connectivity is used to describe how the spatial

arrangements and the quality of elements in the landscape affect the movement of

organisms among habitat patches (Forman 1995). Among other alternatives, corridors are

a strategy for maintaining connectivity in the fragmented landscape (Tewsbury et al.

2002). A number of definitions and types of corridors have been proposed over time

(Forman 1995; Bennett 2003; Hilty et al. 2006; Anderson and Jenkins 2006). For

instance, Forman (1995) defined corridors as strips of habitat that differ from the adjacent

habitat on both sides.

A more detailed definition is provided by Anderson and Jenkins (2006) where

corridors are defined as spaces in which connectivity between species, ecosystems, and

ecological processes is maintained or restored at various levels. In general, habitat

corridors are defined as forested or close-forest corridors; however, species that live in

open habitats might also need open-habitat corridors for movement and dispersal (Asking

1994; Haddad and Tewsbury 2005). For instance, a study of butterflies (Aphantopus

hyperantus) in eastern England found that they used grassy tracks as corridors to move

between glades in dense woodlands (Sutcliffe and Thomas 1995). Haddad and Tewsbury

(2005) found similar pattern for two open-habitat butterfly species Junonia coenia and

Euptoieta claudia in the USA.

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Bennet (2003) classified close-forest corridors as follows:

(1) natural corridors, such as waterways and streams and their associated riparian

vegetations;

(2) remnant corridors, such as strips of unlogged forest within clear-cuts, natural

woodlands along roadsides, and natural habitat retained as links between nature reserves;

(3) regenerated corridors, such as fencerows and hedges; and

(4) planted corridors, such as windbreaks or shelterbreaks and urban greenways.

Regardless the type of corridor, Forman (1995) mentioned that there are six main

functions that corridors provide:

(1) Conduit. A corridor acts as a conduit when it provides for movement between habitat

patches, but organisms do not reside within it (Hess and Fischer 2001).

(2) Habitat. A corridor performs as a habitat when the organisms have enough resources

for survivorship, reproduction, and movement (Hess and Fischer 2001).

(3) Filter. A corridor acts as a filter when there is some level of permeability and some

organisms and material pass through the corridor, whereas others cannot (Hess and

Fischer 2001).

(4) Barrier. A corridor may represent a barrier to animals when it is a complete blockage

and no animals can cross the corridor (Hess and Fischer 2001).

(5) Source. A corridor can work as a source when animals emanate from it (Hess and

Fischer 2001).

(6) Sink. A poorly designed corridor may act as a population sink, because the large

amount of edge exposes animals to predation from matrix dwellers and competition

11
from generalist species (Henein and Merriam 1990; Soulé 1991, cited by Hess and

Fischer 2001).

Although biological corridors can be good tools for biological conservation, there is a

large controversy about their efficacy (Beier and Noss 1998; Tewsbury et al. 2002;

Bennett 2003). Bennett (2003) summarized the critics in three main points:

(1) whether sufficient scientific evidence is available to demonstrate the potential

conservation benefits of corridors;

(2) whether the potential negative effects of corridors may outweigh any conservation

value;

(3) whether corridors are a cost-effective option in comparison with other ways of

using scarce conservation resources (e.g larger reserves).

Even though several disadvantages of corridors have been reported, such as

serving as pathways for fire, predators, and pathogens--which can each undermine

conservation objectives (Simberloff and Cox 1987; Forman 1995; Anderson and Jenkins

2006), and even though it is clear that corridors are not the solution to all of the current

conservation problems (Noss 1987), many of the potential disadvantages could be

avoided or mitigated if the proper design is applied to the specific requirements of the

species, habitats, ecosystems, and ecological processes of concern in each case (Anderson

and Jenkins 2006). However, further research has to be carried out in order to investigate

the positive or negative impacts of corridors, especially at the landscape level.

12
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16
Chapter 2

Physical, Political, and Socio-Economic Aspects of the Path of the Tapir Biological
Corridor

Introduction

The forest cover of Costa Rica has been affected by both natural and human

disturbances throughout its history. Fires, volcano eruptions, and earthquakes have been

documented as major disturbances that have changed vegetation and successional taxa

throughout the country’s history (Horn and Sanford 1992; Anchukaitis and Horn 2005;

Valerio 2006; Meza-Ocampo 2009). Although hurricanes and tropical storms do not

directly strike Costa Rica, indirect effects such as floods and landslides have also

contributed to land-use change in the country, especially on the Pacific coast (Valerio

2006; Meza-Ocampo 2009).

Even though humans have been an important cause of land-use change since they

first appeared, their impact has varied throughout time, and has become more significant

in the last century. For instance, although Costa Rica has been inhabited by humans for

more than 12,000 years (Valerio 2006), the first documented anthropogenic disturbances

on the country’s rainforest have been dated to 3,000 BP (Northrop and Horn 1996;

Clement and Horn 2001; Anchukaitis and Horn 2005).

Results of pollen and charcoal analyses in several locations have depicted that

humans disturbed the landscapes through forest clearance and fires associated with

agriculture (e.g slash and burn agriculture), which were sporadic but destructive

(Northrop and Horn 1996; Clement and Horn 2001; Anchukaitis and Horn 2005). Pre-

Columbian population was estimated to be 27,000 people (Keogh 1984). However, based

on post-Columbian evidence, it is thought that the forest area cleared was less than 2%

17
of the country’s entire area from the sixteenth century (Spanish arrived) through the

eighteenth century (Tosi 1974; Keogh 1984), particularly because of low population

growth (Keogh 1984). Throughout this colonial era, population grew from 15,500 in

1600 to 52,000 in 1800 (Keogh 1984).

In the nineteenth century, coffee production was responsible for most forest

clearance in the central part of the country as well as infrastructure development (e.g

roads – Gomez and Savage 1983). In 1800, cleared agriculture area represented between

3.5 and 5 % of the country and forest cover represented approximately 92 to 93% (Keogh

1984). The country’s forest cover changed most dramatically during the twentieth

century. Until the early 1900s, Costa Rica was still almost entirely covered by rich and

diverse tropical forests (Tosi 1974; Keogh 1984; Harvey et al. 1998; Hall 2000). By

1900, the estimated forest cover in the country was approximately 87 to 90% (Tosi 1974;

Keogh 1984).

Subsequently, as a result of rapid population growth, the forest cover was

estimated to decrease to 76 - 85% of the territory in the 1940s (Sader and Joyce 1988;

Brockett and Gottfried 2001; Kleinn et al. 2002). However, this area decreased further

until loss totaled more than 80 % of the original forest in the 1980s (Brockett and

Gottfried 2001; Kleinn et al. 2002; Joyce 2006). This resulted in part from official

policies that placed a priority on demographic growth and agricultural production

implemented during the 1950s and 1960s (Sanchez-Azofeifa et al. 1999; Brockett and

Gottfried 2001; Pfaff and Sanchez-Azofeifa 2004; Joyce 2006). Population grew

exponentially from 687,000 to 2,044,000 people during the period of 1943 – 1977

(Keogh 1984; INEC 2010).

18
Faced with rapidly disappearing forests, the Costa Rican government responded

with a multifaceted approached. First, the system of national parks was created in the

1970s. Second, a complex regulatory framework governing forestry on privately owned

lands was established through the Forestry Law of 1969 and its revisions of 1973, 1979,

1986, and 1996. Third, financial incentives were provided for reforestation, later for

natural forest management, and most recently for forest preservation (Brockett and

Gottfried 2001).

Over the 1970s and 1980s the greater part of protected areas were created (Kleinn

et al. 2002). Between 1974 and 1978 the areas protected expanded from 3% to 12% of the

national territory, and now stand at around 25-26 % (Pfaff and Sanchez-Azofeifa 2004;

Obando 2007). However, because of the isolation of these protected areas, it was

recommended to implement an appropriate network in order to enhance forest

connectivity (Powell et al. 2000; Sanchez-Azofeifa et al. 2003). This network was

expected to be achieved as part of the Mesoamerican Biological Corridor (MBC), which

aimed to connect most protected areas from Mexico to Panama. The Path of the Tapir

Biological Corridor (PTBC) is a part of the MBC.

This Chapter (2) will present a physical and socio-economic review of the region

as well as an explanation of the goals for the creation of the PTBC. The chapter closes

with a description of the ten different land-use types selected as part of the dissertation

goals, including a description of vegetation types.

19
The Path of the Tapir Biological Corridor

Physical characteristics

The PTBC is located in southwest Costa Rica (Figure 2.1). The corridor’s main

objective is to create a network of sites favorable to fauna and flora between the forests of

the Osa Peninsula and Golfo Dulce, including Corcovado National Park. These forests

connect with those located in the Los Santos Forest Reserve in the Talamanca Mountain

Range. The PTBC area covers approximately 82,000 ha, inhabited by approximately

10,000 people in 55 rural communities. This mosaic of human-dominated land uses

includes primary and secondary forests, native and exotic forest plantations, agriculture,

pastures, bamboo, oil palm plantations, ecotourism projects, and others.

The corridor is composed of terrain ranging in altitude from 0 to 1,100 masl

(TNC-ASANA 2000), and according to the Holdridge System (1967), three life zones are

represented within it: (1) The Tropical Wet Forest that comprises the entire length of the

corridor, especially the lower zones; (2) The Tropical Wet Forest Transition to

Premontane, represented by a small fringe at the intermediate altitudes; and (3) The

Tropical Rainforest Premontane found at the highest elevation in the corridor. The

climate in this region of the country is categorized as Seasonal Tropical Wet with an

annual precipitation of 4,239 mm and average temperature of 27 ºC. There is also a high

precipitation during the rainy season with as much as 685 mm per month (maximum of

1,715 in October 1988), and a pronounced 4 to 5 months dry season with little rain (less

than 100 mm) from January to May (TNC-ASANA 2000). The soils in the corridor are

young, low in fertility, and are generally classified as Ultisols and Inceptisols. There are

more than 30 rivers, among which the main ones are Coronado, Higueron, Uvita, Baru,

Hatillo, Savegre, and Guabo (TNC-ASANA 2000).

20
The PTBC is one of the most diverse regions of Central America because it

represents the transition between the dry forests of the Northeast and the rain forests of

the Osa Peninsula (TNC-ASANA 2000). This part of the country, including the Osa

Peninsula, comprises more than 2.5% of the world’s biodiversity (Obando 2007), with

more than 3000 plant, 173 mammal, 51 amphibian, and 81 reptile species identified in the

corridor (TNC and ASANA 2000, Valenciano 2005). Additionally, 500 avian species

have been registered in the area in the six most recent annual bird counts (Urena, pers.

comm. July 2009). The PTBC provides habitat to some endangered animal species such

as margay (Leopardus wiedii), ocelot (Leopardus pardalis), jaguar (Panthera onca),

spider monkey (Ateles geoffroyi), squirrel monkey (Saimiri oerstedii), scarlet macaw

(Ara macao), great curassow (Crax rubra), and endemic tree species such as quira

(Caryodaphnopsis burgeri). The PTBC region is located in one of the five centers of high

endemism in the country (Obando 2007), with 13 fish, 5 amphibian, 6 plant, 8 reptile, 11

bird, and 1 mammal species enlisted as endemic to Costa Rica.

Land-use in the PTBC

Costa Rican flora and fauna are a fairly recent amalgam resulting from a changing

geography and climate (Rich and Rich 1983; Meza-Ocampo 2009). The continuous

connection between North and South America that it provides has been in existence for

only the past three million years (Meza-Ocampo 2009). Throughout most of the

Pleistocene savanna grassland conditions had a much broader geographic spread in

Central America (Rich and Rich 1983), facilitating species dispersion between North and

South America. However, approximately two million years ago, humid tropical rain

21
forests became widespread in Central America, thus decreasing the effectiveness of the

terrestrial connection (Rich and Rich 1983). Most non-forest species, especially bird

species, persisted in those forested areas utilizing natural light gaps and extensive areas

along rivers that were maintained in early successional stages by periodic floods (Stiles

1983).

In the Holocene (11,300 – 9,600 years), flora was less dense, with some savanna

patches on the Pacific coast as a result of drier and colder weather conditions than at

present (Meza-Ocampo 2009). Subsequently, human disturbances provided more habitats

to non-forest species (Stiles 1983) as described above. The PTBC region had always been

sparsely populated, dating back to the pre-Columbian era (Newcomer 2007), and there is

still physical evidence of these human settlements (Figure 2.2). However, there are no

documented studies of their direct/indirect impacts on forest cover within the PTBC until

more recent post-Columbian times.

The current land use in the PTBC has been the result of the process of local and

national settlement and development policies, as mentioned above. Between 1940 and

1960, Costa Ricans migrated from the northern part of the country toward this region in

the southwest, searching for new lands to clear and cultivate (Newcomer 2007). Over this

period, forest lands were considered worthless on the frontier, and an individual’s

reputation for hard work depended on the amount of land one cleared (Brockett and

Gottfried 2001), thus the principal causes of deforestation were reported to be the

economic demand for land rather than for wood (Hartshorn 1982). On the Costa Rican

frontier, settlers generally occupied land by squatting (Brockett and Gottfried 2001).

22
In the 1970s and 1980s Costa Rica was mainly in the negative environmental

headlines for having one of the highest deforestation rates worldwide. The deforestation

rates consistently averaged two to three times higher than the overall regional average for

Latin America (Wendland and Bawa 1996). Over this period, the forest cover changed

from 49 % in 1969 to only 17 % in 1983 (Sader and Joyce 1988). Between 1960 and

1990, an expanding cattle industry was a major contributing factor to deforestation in the

PTBC (TNC-ASANA 2000).

From the 1990s to date, forest cover has begun to increase as a result of declining

agriculture production in the region, a fall in cattle prices, new environmental laws, and

changing regional demographics (Newcomer 2007, Redondo-Brenes 2007). For instance,

from 1992 to 2000, more than 20,000 ha of pastures were abandoned mainly because of a

decrease in the international beef market. As a result of this land abandonment, there was

an increase in the area under (1) young secondary forests (younger than ten years old), (2)

tree plantations, and (3) the area classified as primary forest (Figure 2.3). From 1997 to

2005, according to Calvo (2010), the PTBC was one of nine biological corridors in the

country that suffered from a high annual deforestation rate (12.5%), however, its net

forest cover and number of forest fragments increased. Deforestation and consequent

land-use change throughout this period was the result of development projects and

changing of forest cover to other agriculture crops such as rice (Figure 2.4). The increase

in net forest cover is likely related to the continued abandonment of pasture lands in the

PTBC, which are naturally regenerating through secondary forest succession.

Aside from anthropogenic disturbances, forest cover in the PTBC has also been

affected by natural events. Earthquakes, floods and landslides are the major natural

23
disturbances in the PTBC. For instance, intense precipitation as a result of hurricane Rita

in September 2005 on the Caribbean coast caused one of the most severe emergencies in

the PTBC in the last 10 years. An area of more than 200 km2 was affected by floods and

landslides (Mendez-Herrera and Esquivel 2006). The large concentration of sediments

along major rivers as well as along the coast exemplifies the indirect effects of hurricanes

and tropical storms during the rainy season on the Pacific coast of the country.

Design, planning, and implementation of the PTBC

Conservation awareness in the PTBC began in the early 1980s, with the creation

of the local NGO ASANA (Friends of Nature from the Central and South Pacific) by

local people being the first step to implement the corridor. ASANA has worked on

conservation issues and developed community-based sustainable projects in the last two

decades. In 1996, the idea of the PTBC was first considered, but it was not until 2000 that

it was officially recognized by Costa Rican authorities. The corridor design encompasses

high elevation lands to protect water sources for local consumption and a matrix of high

and lowlands to protect habitat for hundreds of species. The PTBC is one of the few

projects where a Rapid Ecological Assessment was carried out to justify its importance as

a conservation and development tool in Costa Rica (Ewing, J. pers. comm. July 2006).

The strategy for the creation of the PTBC consisted of three elements:

(1) Encourage land owners to create private biological reserves such as: a) National

Wildlife Refuges like Hacienda Barú and La Merced, b) Informal reserves with

no particular government recognition such as Oro Verde Biological Reserve and

24
Rafiki Safari Lounge, c) Land held in reserve through payment for environmental

services (PES), and d) Land protected by environmental easements.

(2) Encourage and assist landowners in the protection of their reserves. This is being

accomplished through environmental education in surrounding communities, and

by creating covenants through which the National Parks Foundation (NPF) hires

official park rangers, and reserve owners and neighbors reimburse the cost of the

salaries to NPF.

(3) Encourage the creation of natural corridors along rivers, streams and fences in

lands not currently held in reserve, allowing connections between forest patches.

This is being accomplished through environmental education and public

awareness (Ewing, J. pers. comm. 30 October, 2006).

Within their strategy, the PTBC organizations strive to achieve four major goals:

(1) Restore natural habitats to enable the return of terrestrial endangered species and

marine species such as the leatherback sea turtles (Dermochelys coriacea) to the

forests and beaches they inhabited half a century ago, and protect existing species

by allowing local populations to become more robust.

(2) Halt deforestation within the corridor and restore forests in order to complete

connectivity and protect water sources for use by communities, particularly in

watersheds and groundwater recharge zones.

(3) Encourage local communities to value resources and use them sustainably.

(4) Create interconnecting forest reserves between the existing network of forest and

wildlife reserves. Specific conservation programs have been developed by the

25
PTBC organizations to accomplish these goals in the region and they are another

important step in corridor implementation (Anderson and Jenkins 2006).

The main programs implemented by PTBC organizations in the last decade are as

follows:

(1) Environmental education programs in more than 32 schools and workshops for

local adults to build a better understanding of sustainable forest management. In

addition, within the PTBC there are road signs to caution drivers about the

presence of wildlife species and to inform people about the existence of the

corridor.

(2) Promotion of land conservation areas through PES in collaboration with the

government (For more details about PES see Redondo-Brenes and Welsh 2006).

(3) Community-development projects to provide better revenues to local people

through sustainable agricultural practices.

(4) Coordination to develop associations aimed at providing drinkable water to locals

and proper watershed management.

(5) Training and approval of 130 voluntary local game wardens to patrol the regions

ad honorem.

(6) Monitoring and protection of sea turtles and other flora and fauna species. To

date, some of those programs are working well and others still need more funds to

be properly implemented. Despite all these conservation programs, there are

several threats to biodiversity in the region.

26
Threats to biodiversity are development and deforestation, illegal logging, poaching

and hunting, and lack of law enforcement. This is a very attractive area for foreigner

people and tourism projects, and as a result, several real estate developers are buying the

land from locals, cutting the forest to create new roads, and building residential areas,

thus increasing fragmentation. Moreover, even though it is claimed that hunting has

decreased in the last three decades (Ewing, J, pers. comm. June 2006), it is still an issue

and hunters mostly come from communities outside the corridor. Another main constraint

for the PTBC to achieve biological conservation is the lack of funding to support further

projects. The threats to biodiversity grow when we add to the described problems a lack

of law enforcement, interest to control those problems, funds, and in a few cases

corruption from governmental organizations.

Economics

Within the PTBC most local people work in agriculture, and recently ecotourism

has grown to become another important source of income in the region (Newcomer 2007,

Redondo-Brenes 2007). However, as land prices have increased, land ownership is

shifting from local farmers to wealthy foreigners. Costa Ricans have either become

employees of the new owners or migrated to larger cities in Costa Rica or to the United

States and Europe. This poses a new challenge for the region since protected areas are

interspersed with private lands. Costa Ricans have migrated out of the region, and thus

populations have decreased in the four most important districts that share land with the

PTBC (Puerto Cortes, Savegre, Baru, and Bahia Ballena). Even though between 1973 and

2008 there was a 166% increase in population (1.7 to 4.5 million people) in Costa Rica,

27
population decreased 14% from 15,550 to 13,467 people in these four districts, of which

approximately 10,000 inhabit the corridor (INEC 2010).

Agricultural lands in the region are mostly planted with rice, oil palm, and small

scale crops such as maize, cassava, coffee, and beans, and many farmers have

agroforestry combinations of some of these crops with trees and cattle. Pastures for cattle

have different characteristics than cultivated land, as some of them have living fences of

native tree species as well as scattered remnant trees as shade for cattle. Tree plantations

are mostly timber species located in the Caribbean and Pacific lowlands of the country.

The most commonly planted species in this region, respectively, are Tectona grandis

(teak), an exotic species brought to Costa Rica from Asia, Terminalia amazonia

(amarillon), a native species planted in medium or small scale plantations, and Gmelina

arborea (melina), also exotic to Costa Rica. Teak and melina plantations represent more

than 50% of the total area of tree plantations in the country (Chinchilla-Mora and Mora-

Chacon 2002).

Conservation in the region has been undertaken through the establishment of five

National Wildlife Refuges and more than 30 private nature reserves, all of which were

established after 1995 (Ewing, J, pers. comm., June 2006). The participation of local

landowners and their willingness to maintain forest cover will determine the future

success of the PTBC project. The fate of the existing biodiversity in the region depends

on landowners’ management decisions, meaning attractive incentives are necessary to

ensure their engagement in conservation practices (Anderson and Jenkins 2006). The

PTBC organizations help landowners find economic incentives for sustainable land

management (Newcomer 2007; Redondo-Brenes 2007), by providing guidance in

28
obtaining payment for environmental services (PES) from the government (currently

more than 4,500 ha of forest are under protection through PES), funding for community-

development projects, and technical assistance to address water management and other

conservation issues in the region. Additionally, local landowners can benefit from

conserving their lands through ecotourism.

Socio-political issues

In the PTBC almost 100% of the land is privately owned, therefore, decision

making in the region involves many stakeholders (Basso and Newcomer 2009).

According to Newcomer (2002), the PTBC participants can be grouped into three main

in-country clusters: government, community organizations, and landowners. The

government is represented by a local liaison between the PTBC program and Ministry of

Environment (MINAET), and National ministries and municipal government agencies

have direct interests in and influence on the program. The PTBC consists of three

municipalities (Aguirre, Osa, and Perez Zeledon – Figure 2.5), and three conservation

areas (ACOPAC, ACLA-P, and ACOSA – Figure 2.5) led by MINAET. Municipalities

develop zoning plans and provide construction permits within their borders, while the

conservation areas are responsible for the proper management of natural resources in the

country. Currently, only the municipality of Aguirre and ACOPAC (and to a lesser extent

ACLA-P and ACOSA) are supporting the PTBC conservation and development

initiatives. Contrary to the supportive position of these parties, the Mayor of the

municipality of Osa encourages development in the region. In fact, from 2006 to 2007

29
construction permits increased 200% in this county (Redondo-Brenes and Villalobos

2008).

Community organizations include cooperatives, foundations, women’s groups,

environmental groups, agricultural groups, community development associations, and the

PTBC Coordinating Committee. These groups are very active, running most conservation

and community development projects and denouncing any illegal activity against natural

resources in the region. Finally, landowners can be divided into those who participate in

conservation and those who do not. Developers and real estate agencies comprise most of

the non participatory group, which constitutes one of the main threats to biodiversity

conservation in the area. In fact, Basso and Newcomer (2009) reported that more than

71% of people interviewed in the corridor stated their concern about the high rate of real

estate development in the PTBC.

A fourth group not mentioned by Newcomer (2002) consists of individuals and

institutions funding specific conservation and development projects within the PTBC.

Among them are AVINA Foundation, Cedarena Land Trust, Costa Rica Conservation

Trust, the Mesoamerican Biological Corridor Coordinating Committee, and the United

Nations Development Programme (UNDP).

Large-scale conservation projects in private and human-dominated landscapes

require the participation of local people, of which most who necessitate economic

incentives to ensure their support (Anderson and Jenkins 2006). To successfully acquire

local support for the PTBC project, the participants’ needs were taken into consideration

in the corridor’s objectives. For example, since water quality and quantity are important

issues in the region (Welsh 2006), and a water conservation approach has proved to be an

30
effective tool for biodiversity conservation (Redondo-Brenes and Welsh 2006), including

water as a priority in the region was a successful tactic employed by the corridor leaders

to increase local support.

Despite the work that has been done by the PTBC organizations to match

conservation and development in the region, to date, most of the biological data of the

corridor is lacking and further research is necessary to assess the conservation status of

wildlife within this fragmented corridor.

Description of the selected land-use types in the PTBC

The ten land-use types were selected based on several variables. First, available

GIS land-use layers were used to identify the main land-use types in the region, and

second, field work was done to verify the land-use maps (Figure 2.6). Thirdly, interviews

were conducted with local organizations and people to determine what they consider to

be the land-uses of most concern in the region. The fourth factor was the use of Costa

Rican bird guides as well as other studies that have assessed bird diversity in human-

modified landscapes (Stiles and Skutch 1989; Hughes et al. 2002; Peh et al. 2006;

Garrigues and Dean 2007).

At the time of my first visit, the most updated land-use layers were created in

2002 by the National Institute of Biodiversity as part of a project called Ecomapas (INBio

2005). This layer was used as a first step to determine the main land use types in the

region. By 2002, the main land uses in the region were primary and secondary forests

(35,682 ha), pastures (22,243 ha), young secondary forests (13,488 ha), agriculture (4,074

ha), forest tree plantations (2,915 ha), and wetlands (1,160 ha). Based on these land-use

31
types, a few months were spent in 2005, 2006, and 2007, re-classifying each land-use

category in the field and also talking to local organizations. For instance, for the forested

habitats, it was determined that there were four categories of interest: wildlife refuges,

biological reserves, forest edges, and forest fallows. Oil palm plantations and

homegardens were selected as part of the sites classified as agriculture. Two common

human settlements were selected: villages and the new residential tourism projects. For

tree plantations, an exotic (teak) and a native (amarillon) species were selected as will be

described below.

Wetlands, such as major rivers and mangroves, were discarded because of a lack

of accessibility and funding. Access for most rivers needed special permits and in the

case of mangroves the best access was by boat. Therefore, wetlands were considered too

expensive for the dissertation budget. Among the people interviewed were local birders,

staff from ASANA, private reserve’ owners and workers, local tourist guides, and

landowners. In addition, workers from the Minister of Environment, INBio, Neotropical

Foundation, TNC, Universidad Nacional (UNA), and University of Costa Rica were

interviewed.

In summary, based on the four described variables, ten land-use types were

selected as part of this project: wildlife refuges, biological reserves, forest edges, forest

fallows, tree plantations, oil palm plantations, homegardens, residential tourism projects,

villages, and agrosilvopastoral systems.

For the forested habitats (wildlife refuges, biological reserves, forest edges, forest

fallows), seven temporal plots of 15 m-radius were set in order to quantify the vegetation

greater than 5 cm of diameter at breast height (dbh). The seven plots were located at

32
random based on the existing 20 sampling points. Total area sampled by land-use type

was 0.5 ha. In the agrosilvopastoral systems a total of 10 50-m transects were set in order

to determine the trees greater than five cm of diameter planted along living fences and

scattered trees. In the other human-dominated land-use types (homegardens, villages,

residential tourism projects, and oil palm plantations) in ten 50-m radius plots all plants

found were identified. Results of this vegetation inventory is included as part of each

land-use description shown below.

Wildlife refuges

In Costa Rica there are more than 40 legally recognized wildlife refuges that have

been established as part of the national system of protected areas (e.g. national parks).

Wildlife refuges consist of informally protected private nature reserves that, since 1992,

qualify as official national wildlife refuges. Under this program, landowners must

develop a government-approved management plan specifying restrictions of land and

resource use. In exchange, there are three incentives: (1) property tax exemption, (2)

technical assistance for managing the property, and (3) protection against squatter

invasion (Langhloz et al. 2000). In the PTBC there were five wildlife refuges recognized

by 2005: Rancho La Merced, Hacienda Baru, Portalon, Transilvania, and Boracayan.

Rancho La Merced (329 ha) and Baru (330 ha) were selected because of accessibility and

the owner’s willingness to participate in the project. Forested areas (primary or old

secondary forest) were surveyed within the two refuges (10 sampling points at each

refuge for a total of 20 points for this type of habitat).

33
Horizontal and vertical structure of these forests, those in the biological reserves,

and forest edges were characteristic of primary and old-growth secondary forests of Costa

Rica (Figure 2.7; 2.8; Valenciano 2005). The tallest canopy trees were approximately 32

m, and there were trees with diameters of 250 cm. A total of 76 woody species from 31

families with diameters larger than five cm were identified in 0.5 ha sampled plots (Table

2.1). The most abundant plant families were Araliaceae, Tiliaceae, Annonaceae,

Moracea, and Mimosaceae. Moreover, Dendropanax arboreus, Apeiba tiborbou,

Tachigali versicolor, Hyeronima alchorneoides, and Brosimun lactecens were some of

the most common species found in the sampling plots. Brosium utile, Hura crepitans, and

Hyeronima alchorneoides were the species that dominated the canopy, and Apeiba

tiborbou, Tachigalia versicolor, and Dendropanax arboreus dominated the understory.

Tree average basal area at both refuges was 55 m2/ha and volume 620 m3/ha.

Biological reserves

Privately owned reserves continue to attract interest across the tropics for their

ability to blend biodiversity protection with sustainable development (Langholz and

Lassoie 2002). According to Langholz and Lassoie (2002), in Costa Rica there are around

250 private reserves which cover approximately 63,832 ha, or 1.2% of the national

territory. These reserves are protecting ecologically important habitat, particularly

primary rain forest, and they are used for a wide variety of activities, especially

ecotourism and for the owners’ personal enjoyment (Langholz and Lassoie 2002). The

main difference between these private reserves and the wildlife refuges is the legal

34
declaration. Private reserves do not necessarily receive tax exemptions nor receive special

protection from the government.

In the PTBC there are around 30 private reserves. Many of them are used for

ecotourism, but also there are some with restricted access. During my preliminary

assessment of the study region, I visited ten of these reserves. I selected two of these

reserves based on size (the largest ones) and accessibility and in addition, at both

locations ecotourism was practiced as well as in the wildlife refuges. La Cusinga (250 ha)

and Oro Verde (150 ha) were the selected private reserves. Ten sampling points within

each refuge were located. Horizontal and vertical structure of these forests is similar to

the forests of the wildlife refuges (Figure 2.7, 2.8). Sampling points were only located in

areas dominated by primary and/or tall secondary forests. The tallest canopy trees were

approximately 35 m. Ninety nine woody species from 39 families with diameters larger

than five cm were found in 0.5 ha sampled plots.

Tree family composition was also similar to wildlife refuges (Table 2.2).

However, the most abundant families differed between forested habitat types. In the

biological reserves, Mimosaceae, Euphorbiaceae, Sapindaceae, Myristicaceae, and

Lauraceae were the most abundant families. Moreover, tree species composition differed

across wildlife and biological reserves (Table 2.2). Canopy of these forests were

dominated by Hura crepitans, Pterocarpus hayessi, Annona amazonica, Apeiba

membranacea, and Sapranthus palanga. The understory was dominated by Croton

schedianus, Tetrachylachium macrophyllum, Cupania sp, Psycotria sp, and Socratea

exhorriza. Tree average basal area at both reserves was 41 m2/ha and volume 476 m3/ha.

Values were lower than those from the wildlife refuges.

35
Forest edge

The presence and abundance of wildlife species usually differ between forest edge

and interior habitats. Study of forest edges is relevant because there are several forest-

interior species that avoid edges and also there are many open-area species that visit those

habitats (Gascon et al. 1999), making edges highly diverse areas for birds (Stiles and

Skutch 1989). To determine any potential difference in the abundance and composition of

birds across forests and forest edges, twenty sampling points were located in areas along

the edge of primary and old-secondary forests. These forest edges were similar in

structure to the forests sampled in wildlife refuges and biological reserves. The canopy

was slightly shorter than the other forests (28 m) and was dominated by primary forest

species such as Sapranthus palanga, Virola sp, Brosimum utile, Annona sp, and Balizia

elegans. The understory was dominated by primary forest species such as Brosimum sp,

Virola sp, and Ocotea sp, as well as secondary forest species such as Casearia arborea

and Croton schidianus. Also, diameter classes were smaller in forest edges than forest

interior sampling plots (Table 2.1).

Tree species composition was different across the reserves and the edges, but for

tree families similarity index values can be considered high (Table 2.2). Thirty five

different tree families and 93 tree species were identified. The most abundant families

were Euphorbiaceae, Moraceae, Myristicaceae, Mimosaceae, and Tiliaceae. Average

basal area for forest edge stands was 39 m2/ha and volume 386 m3/ha.

Forest fallows (young secondary forest)

For the present study, forest fallows were defined as areas of forest regenerating

in recently abandoned pasture lands (1-5 years after abandonment). These fallows are

36
known as the first stage of tropical secondary succession. Pioneer herbs, shrubs and

climbers invade the site after abandonment (Finegan 1996). Likewise, pioneer tree

species of other ecological guilds colonized the stand (Finegan 1992). For the present

study, 42 woody species from 28 families with diameters larger than five cm were

identified in the seven plots that covered 0.5 ha.

Forest fallows were totally different than the forest interior and edges in tree

structure and composition (Table 2.1, 2.2; Figures 2.7, 2.8). Most of these forest fallows

were dominated by herbaceous bush, shrubs, and a few pioneer trees. The most abundant

tree families were Myrtaceae, Cecropiaceae, Sterculiaceae, Melastomataceae, and

Piperaceae. The understory of these fallows were dominated by Psidium guajaba,

Cecropia obstusifolia, Guazuma ulmifolia, Schefflera actinophylla, and Piper sp. Canopy

trees were mostly E. cyclocarpum, Cecropia obstisifolia, C. insingnis, Guazuma

ulmifolia, and Cordia cymosa. According to the Sorensen index (Table 2.2), similarity

values across fallows and the other three habitats were less than 0.58 for tree families and

0.28 for tree species.

The tallest canopy trees were approximately 13-15 m, with a few remnants that

reach 20 m such as Enterolobium cyclocarpum. Also, even though vertical structure of

forest fallows had a similar inverted J shape to the other forested habitats, forest fallow

size classes were lower (Figure 2.6). Tree basal area for forest fallow stands was 7 m2/ha

and volume 31 m3/ha.

37
Homegardens

The homegardens were traditional Costa Rican, and composed of a combination

of annual/perennial crops, ornamental plants, and timber and fruit trees. The selected

areas had a minimum of a hectare of land under this system. Most sampling points were

located in small rural villages such as San Buenaventura, Coronado, and Silencio where

this type of agroforestry system is still a part of the landscape.

Assessing the area around a radius of 50 meters from the sampling point center, a

total of 65 plant species from 34 families were identified within this habitat. The most

common crops were banana (Mussa sp), maize (zeea mais), papaya (Carica papaya), and

cassava (Manihot sculetum). Tree species were located in three main groups: timber,

ornamental, and fruit species. Among the timber species, Cedrela odorata, Samanea

saman, Enterolobium cyclocarpum, and Tabebuia rosea were some the most common

native species. Nevertheless, some exotic species such as teak (Tectona grandis) and

melina (Gmelina arborea) were seen as part of the homegardens. Fruit trees seemed to be

the most commonly used tree species in these selected sampling areas. The most common

fruit trees were mango (Magnifera indica), guava (Psidium guajava), several species of

citrus, several species of Inga spp, start tree (Averroa carambola), among others. For

ornamental purposes, Costa Ricans used Heliconia spp, palms, as well as tree species

such as beach almond (Terminalia catappa), chumico (Schefflera actinophylla), and poro

(Erythrina poepiggiana).

38
Agrosilvopastoral systems

Most of the pastures in the region were used to raise beef cattle and had mostly

been planted with exotic pasture species. At the time of this study, all of the selected

sampling sites were under used (e.g. cattle grazing). Moreover, all sites had either living

fences or scattered trees that provide perches or food sources for birds. Using line transects

in 10 out of 20 sample points, a total of 41 different woody species (28 families) were

identified with a diameter larger than five cm.

Tree species varied in composition and structure from site to site. Some sampling

points were single-species living fences, however, the majority of pasture lands had more

than one tree species planted. Diameter sizes varied from 3 cm to 76 cm. Tree height also

varied, from 2 m to 25 m. The most common tree species used were Bursera simaruba,

Gliricidia sepium, Erythrina poepiggiana, Tabebuia rosea, Enterolobium cyclocarpum

and Cupania guatemalensis.

Tree plantations

Most tree plantations in the PTBC consist of teak (Tectona grandis) and amarillon

(Terminalia amazonia). Teak is one of the most important tropical hardwood species in

the international high-quality timber market (Bermejo 2004), mostly exported to Europe

and the United States. It is native to India, Myanmar (Burma), Thailand and Laos, but

this broadleaved tree species now grows in the entire inter-tropical region (excluding

desert areas of Africa- Bermejo 2004). In Costa Rica more than 40,000 ha were planted

with teak in the lowlands of both the Pacific and Caribbean regions in the last two

decades (Kanninen et al. 2004).

39
These plantations are the first serious reforestation projects under intensive

silvicultural management. Teak has since acclimatized well and has been widely grown

in both industrial plantations and small community woodlots (Bermejo 2004). In the

PTBC there are both industrial plantations and small-scale reforestation programs,

however, management intensity at both ends of the spectrum is similar. Most plantations

that were visited did not have any understory regeneration. However, in some cases,

remnant trees and living-fences of native species were seen as part of these monocultures.

Amarillon is native to Costa Rica, and is one of the most promising species for

timber production in the country (Streed et al. 2006; Redondo-Brenes 2007; Calvo et al.

2007). Terminalia amazonia can be found naturally throughout Central America, ranging

from Mexico to South America and the Antilles, and throughout Costa Rica and much of

Central America, it has commonly been used within hardwood plantations (Jimenez et

al. 2002). The T. amazonia species is a promising plantation species because it can thrive

in almost all types of soils, it has an average growth of five m in height and 5.8 cm of

diameter after only three years in plantation, and the average survival rate within

plantations in the northern part of Costa Rica is 85% (Jimenez et al. 2002). Previous

research even suggests that T. amazonia is the most adapted native hardwood species for

survival in eroded soils (Carpenter et al. 2004).

In the PTBC, T. amazonia plantations were mostly established with government

incentives, and most were a part of small-scale reforestation programs. Several of them

established with purposes other than timber production such as restoration of degraded

landscapes. Silvicultural management of amarillon plantations differed from teak

plantations in that they did not have a defined management plan like teak plantations did.

40
Most amarillon plantations contain a dense understory dominated by herbaceous and

woody tree species.

Overall, amarillon and teak plantation sizes varied from 2 ha to 30 ha, with teak

plantations being the largest. Tree diameters varied from 9 cm to 30.5 cm and height

varies from 12 m to 22.5 m, with the teak trees having the largest overall sizes. Since

there was not enough T. amazonia to set up 20 sampling points, ten points were located in

teak and ten in amarillon plantations in order to have a total of 20 points for this habitat

type.

Oil palm plantations

In the northern region of the corridor, there were hundreds of ha of oil palm

plantations (Elaeis guineensis), which is an exotic crop to Costa Rica. All plantations

belong to Coopesilencio, a local farmers’ cooperative with more than 600 ha of oil palm

in the region. Most of them have either living fences or a few scattered trees as part of

their land-use type. The most common tree species found were Gliricidia sepium,

Guazuma ulmifolia, Enterolobium cyclocarpum, Cordia alliodora, Cecropia sp, among

others. Aside from the tree species mentioned above, natural grasses and bushes are also

part of the landscape, especially for young plantations before the canopy closes (4 m tall).

However, most grasses are manually eliminated as part of the plantation maintenance.

Many granivore bird species are found visiting young plantations.

In the Silencio community 400 people depend mainly on their palm plantations

located on the community’s 1,100 ha landholdings. The harvest season is from April to

November, and from December to March, the plantation is in reproduction mode to get

41
ready for the new harvest. To maintain their crop, different sections of the plantation are

harvested every year to ensure the sustainability of their crop. One hundred and forty

three palms are planted per ha. The life cycle of these plantations is around 20 years

when plantations reach ten meters in height. Maximum yields are obtained between 5-15

years. The sampling points were located in a range from recently established plantations

(1.5 m tall) to mature plantations (up to ten m height).

Residential tourism projects

Because the PTBC is along the Central and South Pacific Coast of the country,

there has been an exponential growth in the number of foreigners building summer or

retirement houses in the area in the last ten years. Most people live here for one or a few

periods throughout the year, and only a minority of people occupy their houses year

round. The sampling points were located in areas where more than one house was built.

Houses in residential tourism projects were mostly surrounded by forested habitats, but

most keep at least a 30 m distance between forest and the infrastructure. They were

located in different locations along the PTBC such as Ojochal, Escaleras, Lagunas,

Portalon, and Pasito. These houses were two to three times larger than houses in villages

or those with homegardens. Most of them also included exotic plant species, such as

palms, as part of their landscaping.

Regarding plant diversity, a total of 47 plant species from 33 families were

identified within the sampling points. Some of the common tree species were Tabebuia

rosea, Guazuma ulmifolia, Ficus sp, Citrus sp, Cecropia sp, and E. cyclocarpum.

42
Villages

Two main areas were selected for sampling. The first one was the largest village

within the corridor, Puerto Cortez, and here 10 sampling points were selected. The other

10 sampling points were located in the small villages along the main paved highway:

Uvita, Dominical, Hatillo, and Matapalo. Most sampling areas were a combination of

residential and commercial buildings. Construction area and population density in the

villages was greater than in homegardens or residential tourism projects.

Vegetation of these villages was a combination of native and exotic plant species.

A total of 57 plant species from 34 families were identified within the sampling points.

Some of the common plant species found in these habitats were Terminalia cattapa,

Mangifera indica, Coccos nucifera, and Ficus sp.

43
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48
Table 2.1 Summary of vegetation data for five land-use types in the Path of the Tapir
Biological Corridor, Costa Rica.

Wildlife Biological Forest Forest Tree


Refuge Reserve Edge Fallow Plantations
Families (N/0.5 ha) 31 37 37 27 2
Species (N/0.5 ha) 76 99 93 42 2
Densities (N/ha) 768 868 688 562 787
Diameter (cm) 18.3 16.6 18.7 10.2 22.9
Height (m) 9.2 9.8 10.4 5.0 20.4
Basal Area (m2/ha) 55.2 40.6 38.7 6.8 26.7
Volume (m3/ha) 629.8 476.6 386.5 30.6 272.9

Table 2.2 Sorensen Similarity Index for tree species (bold) and tree families in four land-
use types in the Path of the Tapir Biological Corridor, Costa Rica.

Biological
Reserves Forest Edge Forest Fallow Wildlife Refuges
Species
Biological Reserves 0.552 0.269 0.571
Forest Edge 0.777 0.281 0.532
Forest Fallow 0.593 0.58 0.237
Wildlife Refuges 0.805 0.738 0.596
Families

49
Figure 2.1 Location of the Path of the Tapir Biological Corridor, Costa Rica

50
Figure 2.2 There is physical evidence that indigenous people settled a few locations on

the PTBC. These petroglyphs were found in a farm in the central part of the Corridor. (A)

represents a whale, (B) a turtle, and (C) a more sophisticated map. Photos by Alvaro

Redondo-Brenes.

51
45000 1992
2000
40000

35000

30000

25000
Area (ha)

20000

15000

10000

5000

0
Tree Infraestructure Young Mangrove Agriculture Forest Pastures
plantations Secondary
Forest

Figure 2.3 Land-use change from 1992 to 2000 in the Path of the Tapir Biological

Corridor, Costa Rica. Layer Source: INBio (2005)

52
Figure 2.4 Illegal logging and burning of mangrove forest found on a property in Hatillo

of Aguirre, Puntarenas, Costa Rica. Photo taken in April 2010 by A. Redondo-Brenes.

53
Figure 2.5 Political division of the Path of the Tapir Biological Corridor in three

Conservation Areas (ACOPAC, ACOSA, and ACLA-P) and four counties (Osa, Aguirre,

Perez Zeledon, and Dota).

54
Figure 2.6 Land-use types in the Path of the Tapir Biological Corridor in 2000, Costa

Rica. In this black & white version dark colors represent forested habitats and light colors

human-modified land-use types.

55
250

Biological Reserve
Wildlife Refuge
200 Forest Edge
Forest Fallow
Tree Plantation

150
Number of trees

100

50

0
5-10 15-20 25-30 35-40 45-50 55-60 65-70 75-80 85-90 115-120 130-135 160-165 245-250

Diameter (cm)

Figure 2.7 Diameter size class distribution of tree species located in five land-use types in

the Path of the Tapir Biological Corridor, Costa Rica

56
200 Biological Reserve
Wildlife Refuge
180 Forest Edge
Forest Fallow
160
Tree Plantations
140
Number of Trees

120

100

80

60

40

20

0
0-5 5-10 10-15 15-20 20-25 25-30 30-35
Height (m)

Figure 2.8. Total height size class distribution of tree species located in five land-use

types in the Path of the Tapir Biological Corridor, Costa Rica

57
Chapter 3

Avian Diversity of Ten Different Land-use Types in a Human-Modified Biological


Corridor in Costa Rica: Implications for Land-Use Planning

Abstract

As a result of the limitations of current protected area systems and forested areas

in providing habitat for most wildlife species, in the last two decades efforts have shifted

to studying wildlife conservation in human-modified landscapes. The present study was

carried out in the Path of the Tapir Biological Corridor, Costa Rica. The corridor, an

82,000 ha area of fragmented forests, encompasses 55 rural communities with more than

10,000 people, and is considered one of the most diverse regions on the Pacific Coast of

Central America. However, deforestation and development are threatening this high

biodiversity. The main objective of this chapter is to describe the contribution to bird

biodiversity conservation of ten different habitat types in the corridor: wildlife refuges,

biological reserves, forest edges, forest fallows, tree plantations, agrosilvopastoral

systems, homegardens, oil palm plantations, villages, and residential tourism projects.

Bird data were obtained using point counts during a two-year period. Each habitat type

had 20 sampling points (200 total), and each point was visited six times during dry

seasons and six times during rainy seasons. Overall, 44, 917 birds from 48 families and

334 species were identified in this study. Forested land-use types had the highest number

of bird species (81%). Very important, 77% of the birds registered were also found in the

human-modified land-use types. In general, it is concluded that forested habitats should

be the priority areas for conservation at the landscape level because they provide the main

habitat for the most species. Moreover, in human-modified landscapes forest fallows,

58
agroforestry systems, and native tree plantations can be incorporated in land-use planning

strategies to provide additional habitat to forest-dependent and non-forest depend species,

and connectivity to the otherwise isolated and fragmented forests.

Introduction

Destruction or alteration of natural habitat because of land-use change represents

one of the most serious threats to biodiversity worldwide (Groom et al. 2005) along with

climate change and invasive species (Sala et al. 2000). As a result of this loss of natural

habitats, maintaining and conserving biodiversity in fragmented landscapes now

dominated by human land use is a challenge (Bennett 2003; Chazdon et al. 2009a).

Assessing the conservation potential of human-dominated landscapes requires

investigation of the activities, movement, and persistence of species not only in remnants

of native habitats but also in the full array of countryside habitats (Saunders et al. 1991;

Daily 2001; Hughes et al. 2002; Chazdon et al. 2009a), known also as the matrix. The

matrix can be defined as the most widespread habitat within which other elements are

embedded, and it can be either the original habitat type (e.g., a primary forest now

surrounded by a matrix of agroforestry) or a modified one (e.g., an agricultural plantation

surrounded by a matrix of pristine forest) (Anderson and Jenkins 2006). In

anthropogenically modified landscapes, some or all of the matrix may be human-

modified communities such as agricultural fields of various types, agroforestry systems,

clear-cut forests, pastures, tree plantations, fallow land, and towns (Daily et al. 2003;

Hilty et al. 2006).

59
Conserving biodiversity should incorporate human-modified landscapes in

assessments of biodiversity and ecosystem services, planning of corridors, establishment

of buffer zones, and restoration of degraded lands (Chazdon et al. 2009a). Understanding

the contribution of the different land-use types within a landscape will be important for

land-use planning, especially in areas with high biodiversity concerns and high human

impact.

The present study was carried out in the fragmented and human-modified Path of

the Tapir Biological Corridor in Costa Rica (PTBC), which is one of the most diverse

areas of Central America (TNC and ASANA 2000), but whose biodiversity is at risk

because of deforestation and development. Current land use in the corridor has been the

result of local and national settlement and development policies (Newcomer 2006;

Redondo-Brenes 2007). Between 1940 and 1960, Costa Ricans migrated from the

northern part of the country toward this region searching for new lands to clear and

cultivate. Between 1960 and 1990, an expanding cattle industry was a major contributing

factor to deforestation (TNC and ASANA 2000). Recently, deforestation rates have

decreased, forest cover has increased as a result of pasture abandonment, and

conservation efforts are being undertaken through the establishment of a National Park,

five National Wildlife Refuges, and 27 Informal Private Nature Reserves (Redondo-

Brenes 2007). However, as land prices have increased, land ownership is shifting from

local farmers to wealthy foreigners; and infrastructure development is growing

uncontrolled. These changes pose new challenges for the region, since protected areas are

interspersed with private lands (Redondo-Brenes 2007).

60
The main goal of this study was to assess the contribution of ten different habitat

types to the conservation of bird species in the PTBC. The ten land-use types were:

biological reserves, wildlife refuges, homegardens, agrosilvopastoral systems, forest

edges, forest fallows, tree plantations, oil palm plantations, local villages, and residential

tourism projects. This information will be important for assessing the current status of

bird species in the corridor as well as the conservation value of the different habitat types

for land-use planning strategies.

Methods

Study Area Description: Path of the Tapir Biological Corridor (PTBC)

The PTBC is located in southwestern Costa Rica (Figure 3.1) and is a part of the

multinational Mesoamerican Biological Corridor (MBC). The corridor’s main objective

is to create a network of sites favorable to fauna and flora between the forests of the Osa

Peninsula and Golfo Dulce, including Corcovado National Park. These forests connect

with those located in the Los Santos Forest Reserve in the Talamanca Mountain Range.

The PTBC area covers approximately 82,000 ha and is inhabited by 10,000 people in 55

rural communities. This mosaic of human-dominated land uses includes primary and

secondary forests, native and exotic forest plantations, agriculture, agroforestry systems,

bamboo, oil palm plantations, ecotourism projects, and others.

The corridor is composed of terrain ranging in altitude from 0 to 1100 meters

above sea level (TNC and ASANA 2000). According to the Holdridge System (1967),

three life zones are represented within it: (1) The Tropical Wet Forest that comprises the

entire length of the corridor, especially the lower zones; (2) The Tropical Wet Forest

61
Transition to Premontane, represented by a small fringe at the intermediate altitudes, and

(3) The Tropical Rainforest Premontane found at the highest elevations in the corridor.

The climate is categorized as Seasonal Tropical Wet with an annual precipitation of 4,239

mm and average temperature of 27 ºC. There is high precipitation during the rainy season

with as much as 685 mm per month (maximum of 1,715 in October 1988), and a

pronounced 4- to 5- month dry season with little rain (less than 100 mm) from January to

May (TNC and ASANA 2000). The soils in the corridor are low in fertility, and are

generally classified as Ultisols and Inceptisols. There are more than 30 rivers among

which the main ones are Coronado, Higueron, Uvita, Baru, Hatillo, Savegre, and Guabo

(TNC and ASANA 2000).

PTBC is one of Costa Rica’s most diverse regions. A total of 2700 plant, 173

mammal, 51 amphibian, and 81 reptile species have been identified in the corridor (TNC

and ASANA 2000). Moreover, 500 avian species have been registered in the area in the

six most recent annual bird counts. The PTBC provides habitat to some endangered

animal species such as margay (Leopardus wiedii), ocelot (Leopardus pardalis), jaguar

(Panthera onca), spider monkey (Ateles geoffroyi), squirrel monkey (Saimiri oerstedii),

scarlet macaw (Ara macao), great curassow (Crax rubra), and endemic tree species such

as quira (Caryodaphnopsis burgeri).

Description of the Habitats Used for Evaluation of Bird Abundance and Diversity

Based on the predominant land uses currently present in the PTBC, ten different

habitat types, located up to 500 m.a.s.l., were selected. The studied habitat types were

selected based on accessibility, availability, and importance within the corridor landscape

62
among others. In the case of the wildlife refuges and biological reserves, they were also

chosen based on their importance as core areas for wildlife conservation within the

corridor, as well as owner’s permission to get access to the properties. A complete land-

use type description can be found in Chapter (2).

(a) Wildlife refuges: Forested areas (primary or old secondary forest) were surveyed

within two refuges: Rancho La Merced and Hacienda Baru (10 sampling points at each

refuge for a total of 20 points for this type of habitat). La Merced (329 ha) and Baru (330

ha) are private reserves and have had governmental protection since 1995. Average basal

area at both refuges was 55 m2/ha and volume 620 m3/ha. In addition, 76 woody species

from 31 families with diameters larger than 5 cm were identified in 0.5 ha sampled area.

The tallest canopy trees were approximately 32 m.

(b) Biological reserves: Two biological reserves were surveyed: La Cusinga and Oro

Verde (10 sampling points within each refuge). La Cusinga (250 ha) and Oro Verde (150

ha) are private reserves without governmental incentives or protection. Average basal

area at both reserves was 41 m2/ha and volume 476 m3/ha. Additionally, 99 woody

species from 39 families with diameters larger than 5 cm were found in 0.5 ha sampled

area. The tallest canopy trees were approximately 35 m.

(c) Forest edge: Twenty sampling points were located in areas along the edges of

primary and old-secondary forests. Average basal area for forest edge stands was 39

m2/ha and volume 386 m3/ha; 93 woody species from 35 families with diameters larger

than 5 cm were identified in 0.5 ha sampled. The tallest canopy trees were approximately

28 m.

63
(d) Forest fallows (young secondary forest): These were areas of forest

regenerating in recently abandoned pasture lands (1-5 years after abandonment). Average

basal area for forest fallow stands was 7 m2/ha and volume 31 m3/ha. Moreover, 42

woody species from 28 families with diameters larger than 5 cm were identified in 0.5 ha

sampled. The tallest canopy trees were approximately 13-15 m, with a few remnants that

could reach 20 m.

(e) Homegardens: These were traditional Costa Rican homegardens composed of a

combination of annual/perennial crops, ornamental plants, and timber and fruit trees. By

assessing the area around a radius of 20 meters from the sampling point center, a total of

65 plant species from 34 families were identified within this habitat.

(f) Agrosilvopastoral systems: Most of the pastures in the region are used to raise

beef cattle and are mostly planted with exotic pasture species. All of the selected sites had

either living fences or scattered trees that provided perches or food sources for birds. Using

line transects in 10 out of 20 sample points, a total of 41 different woody species (28

families) larger than 5 cm of diameter were identified, either as living fences or scattered

trees.

(g) Tree plantations: Most tree plantations in the PTBC consist of teak (Tectona

grandis) or amarillon (Terminalia amazonia). Teak is a valuable exotic timber species

(native to Southest Asia) that is exported to Europe and the United States. Amarillon is

native to Costa Rica and is one of the most promising species for timber production in the

country. Since we did not get access to enough T. amazonia plantations to set up 20

sampling points, 10 points were located in teak and 10 in amarillon plantations in order to

have a total of 20 points for this habitat type. Plantation sizes varied from 2 ha to 30 ha

64
with teak plantations being the largest. Tree diameters varied from 9 cm to 30.5 cm and

height from 12 m to 22.5 m, with the teak trees being the largest overall.

(h) Oil palm plantations: In the northern region of the corridor, there were hundreds

of ha of oil palm plantations (Elaeis guineensis), which is an exotic crop to Costa Rica.

The sampling points were located in a range from recently established plantations (1.5 m

tall) to mature plantations (up to 10 m height).

(i) Villages: Two main areas were selected for sampling. The first one was the

largest village within the corridor, Puerto Cortez, where 10 sampling points were

selected. The other 10 sampling points were located in the small villages along the main

highway. A total of 57 plant species from 34 families were identified within the sampling

points.

(j) Residential tourism projects: Because the PTBC runs along the Central and

South Pacific Coast of the country, there has been an exponential growth in the number

of foreigners building summer or retirement houses in the area in the last 10 years. The

sampling points were located in areas where there was more than one house built. A total

of 47 plant species from 33 families were identified within the sampling points.

Bird Surveys

Point counts were used because they allow one to develop relative indices of

abundance and inferences about bird-habitat relations (Buckland et al. 1993; Bibby et al.

2000; Blake and Loiselle 2001; Sutherland 2006; Barlow et al. 2007; Farwing et al.

2008). The primary advantages of point counts are that the relative abundance of many

species can be determined over broad areas at a moderately low cost and that species-

65
habitat relations can be evaluated effectively compared to other methods (Bibby et al.

2000; Sutherland 2006). For the present study, 20 point counts were located within each

habitat site in 16 sampling routes. Each route was selected based on previous visits to the

area, in an attempt to minimize cost. The minimum and maximum number of sampling

points per route were ten in forested habitats and 15 in more open-habitats. Average

minimum distance in between points was 200 m in forested habitats, and 250 m in open

areas to avoid double-counting the same individual (Bibby et al. 2000; Sutherland 2006).

Each point was surveyed three times in the dry and three times during the rainy

seasons over a two year period (12 visits per sampling point total). Dry season surveys

were conducted from mid-January to mid-April and rainy season surveys from mid-June

to mid-August. At each sampling point, every bird species that was seen or heard within a

50m radius plot and during a period of 10 minutes was recorded and identified. All

surveys were conducted from sunrise to 9:15 am during clear days, avoiding windy

situations. The daily order of point sampling in a route was changed so that each point

was visited once in the first hour, once in the second hour, and once in the third hour of

the season sample period. Field identification was conducted using the Manual of Birds

of Costa Rica (Stiles & Skutch 1989) and the Birds of Costa Rica (Garrigues & Dean

2007), as well as an identification of their calls and songs. All bird identifications were

done by A. Redondo-Brenes. Total observation time was 400 hours for the whole study

(2 hours/point).

66
Data Analysis

For each habitat type the total abundance and species richness of birds were

calculated by combining data from the two sampling periods (dry and rainy) as well as by

comparing between the two years considered for this study. Shannon diversity index,

rarefaction curves, Sorensen similarity index, and the number of shared species using

EstimateS 5.0 were computed (Colwell 2005). Rarefaction curves were plotted against

the number of individuals observed, using the mean of the four commonly employed

abundance-based estimators (ACE, CHAO1, JACK1, and BOOSTRAP; Barlow et al.

2007). Abundance, species richness, and diversity among the ten land-use types were

compared, using analysis of variance and/or Kruskal Wallis tests. Cluster analysis was

also used to group habitat types based on species composition. All statistical analyses

were conducted in PAST v 1.95 (Hammer et al. 2001) and SAS v. 9.2.

Results

Bird Diversity

A total of 44,917 birds, 48 families, and 334 bird species were identified over the

two-year period of this study (Appendix 1). From the total number of observed birds,

21,025 individuals (293 species) were recorded in 2008 and 23,902 (310 species) were

recorded in 2009. As expected, there were differences in the accumulated total number of

species found during dry (307 species) and rainy time (271 species) (Figure 3.2).

However, even though the total difference across both seasons was 36 species, there were

63 species that were only recorded over dry surveys and 27 species only recorded during

rainy surveys. From the 27 species found only in the rainy, 26 species are considered rare

or uncommon species. In fact, only the Dendrocygna autumnalis had abundance greater

67
than 5 individuals for the entire study (73 birds). On the other hand, of the 63 species

only found in the dry period, 46 species (73 %) were neotropical migratory species and

17 species were resident species. Migratory species accounted for 13.7% of the total bird

diversity registered in the PTBC.

Comparing overall abundance at the species level, it was found that while 20

species had more than 50% of the entire records for this study, there were 135 species

(40% of all species) whose sightings averaged less than one for each of the 12 surveys

conducted. Moreover, there were 57 species (17%) that had just one or two individuals

recorded in 2 years. The most common species for this study were Ramphocelus

costaricensis, Quiscalus mexicanus, Sporophila americana, Thraupis episcopus,

Troglodytes aedon, Pitangus sulphuratus, Volatinia jacarina, Brotogeris jugularis,

Tyrannus melancholicus, and Thraupis palmarum. Of the total birds recorded for this

study, these species comprised from 4.7% to 2.5% of the whole abundance. Quiscalus

mexicanus had a population that varied from 743 birds in 2008 to 1001 birds in 2009 - a

34% change.

Bird abundance across the 10 habitat types

At the family level, data among the ten habitat types varied from 39 bird families

in wildlife refuges/homegardens to 31 families in the oil palm plantations. Although this

difference across land-use types is only eight families, the significant difference is at the

species composition level. Overall, five species account for 50 % or more of the total

number of individuals per land-use type (Figure 3.3). Twenty two families were

68
observed in all land-use types and the most abundant were Thraupidae (14% of the total),

Tyrannidae (13%), Emberizidae (8%), Psittacidae (7.4%), and Columbidae (7%).

At the landscape level, homegardens, agrosilvopastoral systems, and villages had

the highest bird abundance; tree plantations had the lowest (p < 0.05; Table 3.1). Forested

habitats (i.e. biological reserves, wildlife refuges, forest edges) also had low bird density

values. Moreover, whereas forest edges, forest fallows, homegardens, biological reserves,

and wildlife refuges were the sites with the highest species richness and diversity of

species, tree plantations, residential tourism, oil palm plantations, and villages had the

lowest diversity values within the biological corridor. The latter two were statistically the

least diverse sites of the ten land-use types assessed (p < 0.05).

Based on the 2-year accumulated data, rarefaction curves confirmed some of the

diversity patterns described above (Figure 3.4). In summary, forest edges, forest fallows,

biological reserves, and wildlife refuges are expected to accumulate the largest number of

species, followed by homegardens, tree plantations, and agrosilvopastoral systems. By

contrast, residential tourism projects, oil palm plantations, and villages seemed to have

the lowest expected number of species.

Species composition also varied across the ten habitat types in the corridor.

Biological reserves, wildlife refuges, and forest edges had the most similar assemblages

of species (Table 3.2, Figure 3.5). This may be because these habitats were dominated by

primary and old-secondary forests, having a majority of forest-specialist bird species

(Redondo-Brenes and Montagnini 2010; see also Chapters 2 & 4). Also, tree plantations

seemed to share many species with these three habitat types. Agrosilvopastoral systems,

homegardens, residential tourism projects, and oil palm plantations had similar

69
assemblage of species because they were dominated by generalist and open area bird

species (Chapter 4). In contrast to these patterns of high similarity, more open area

habitats (i.e. villages, oil palm plantations, residential tourism projects) tended to have the

lowest similarity indexes in relation to forested biological reserves, wildlife refuges, and

even forest edges.

At the species level, of the 334 species recorded, only 10% of these species (33

species) were found in all ten habitat types (Appendix 1), confirming the highly distinct

bird assemblages across the land-use types. The majority of these species (26 species –

76%) corresponded to resident species, and only seven were migratory species:

Empidonax flaviventris, Piranga rubra, Legatus leucophaius, Dendroica pensylvanica,

Vermicola peregrina, Vireo philadelphicus, and Catharus ustulatus. Contrary to the

adaptation capability of most of these species to different habitat types, there were 61

species (18% of the total diversity) that were only found in one particular land-use type.

There were nine in biological reserves, eight in forest edges and agrosilvopastoral

systems, seven in forest fallows and homegardens, six in wildlife refuges, villages and oil

plantations, and only two in residential tourism projects and tree plantations.

Finally, there were 270 species (81%) sighted in forested habitats, including

biological reserves, wildlife refuges, forest fallows, and forest edges. Also very

importantly, 77% of the total species observed (257 species) were recorded within the six

human-modified land-use types. Furthermore, 66 species (18%) were only found in

human-modified landscapes and 77 species (23%) were only recorded in forested

habitats.

70
Discussion

Bird species identified as part of this study corresponded to almost 40% of the

avian diversity in the country and more than 66% of the expected bird diversity in the

region. Most of these bird species were located in forested habitats; however, the human-

modified landscapes provided habitat to more than 77% of the species found during the

2-year study. This 77% is a value higher than other studies that estimated the contribution

of countryside land uses to landscape biodiversity (Hughes et al. 2002). Because of a

generalized interest in understanding the contribution of human-modified land-use types

to biodiversity conservation (Daily et al. 2003; Chazdon et al. 2009a; Gardner et al.

2009), the following section will discuss the contribution of these habitats to avian

diversity. It will focus on the conservation value these habitats shared with forested

habitat, but understanding that human-modified land use types are also very important for

the overall biodiversity of a region, as these landscapes provide habitat and food sources

to most open-area specialists and to many forest-generalist species.

Secondary forests

In the present study, forest fallow was the human-modified land-use type with the

highest bird diversity and also the greatest bird species similarity with forested habitats.

The young secondary forests (forest fallows) shared 143, 106, and 109 species with forest

edges, wildlife refuges, and biological reserves, respectively (Table 3.2). Secondary

forests may play an important role in biodiversity conservation by increasing regional-

scale species richness at the landscape level (Hughes et al. 2002; Barlow et al. 2007,

Chazdon et al. 2009b), improving connectivity across the landscape, and buffering

71
existing forest fragments (Fischer et al. 2006; Chazdon et al., 2009a). In the PTBC,

young secondary forests are mostly growing in former pasture and agricultural

landscapes surrounding most of the private reserves.

Secondary forests are rapidly expanding across tropical landscapes (Barlow et al.

2007). FAO (2007) reported that the area of secondary forests throughout the world was

increasing dramatically and that in many tropical countries they exceeded areas covered

by primary vegetation. In Costa Rica, there were approximately 400 000 to 450 000 ha of

secondary forests in different successional stages in the 1990s (CCT 1991, Segura et al.

1997, Müller and Solís 1997). This area is twice as large as the area of primary forests for

production objectives and three times the size of tree plantations in the country (Berti

2001). The area under secondary succession has continued to increase from the 1990’s to

date, with a gain in forest cover from 42% in 1997 to 51% in 2005 (FAO 2007). A similar

pattern was found in the PTBC. At present, around 17% of area in the PTBC is under

forest fallows (Redondo-Brenes 2007).

Even though forest fallows can provide habitats for many bird species, regaining

the complex microhabitats and structures required by primary forest specialists is likely

to take centuries (Chazdon 2003; Montagnini 2008; Chazdon et al. 2009b). Dunn (2004)

found that species richness of many taxa may recover relatively rapidly in secondary

forests, but species composition can take longer, especially for ant and bird species.

When these secondary forests are acting as buffer zones or are located near primary

forests, bird species richness can be even higher (Blake and Louis 2001). Primary forest

bird species usually are not found in young secondary forests, limiting the value of these

forests as a conservation tool (Dunn 2004; Barlow et al. 2007). In the current study, 67

72
forest specialist species were recorded in the forest fallows (See Chapter 4), being the

highest of all the human-modified land uses.

Tree plantations

Tree plantations can also provide suitable habitats for many bird species.

However, as in young secondary forests, there is a limited number of forest-dependent

species that usually inhabit them (Carnus et al. 2006; Barlow et al. 2007; Brockerhoff et

al. 2008). In the present study, tree plantations shared 97, 96, 125 species with wildlife

refuges, biological reserves, and forest edges, respectively (Table 3.2). Tree plantations

had 55 forest-specialist species (Chapter 4). These values are lower than those from forest

fallows, but the second highest for the seven human-modified habitats in this study.

Tree plantations can enhance local biodiversity by promoting the regeneration of

understory species through shading out grasses, increasing nutrient richness of topsoil,

allowing the growth of more sensitive tree species, and creating a microclimate that

attracts seed dispersers (Cusack and Montagnini 2004; Montagnini 2010). In addition,

tree plantations may serve as perches, food sources and habitat for a number of wildlife

species, thus contributing to an increase in overall biodiversity (Slocum and Horvitz

2000; Slocum 2001; Carnus et al. 2006).

Use of native species, especially in mixtures, may increase wildlife populations in

former degraded landscapes (Lamb and Gilmour 2003). Recent studies conducted in

experimental plantations of several native species in Costa Rica have found abundant and

species-diverse understories in these plantations (Orozco and Montagnini 2007; Butler et

al. 2008; Leopold and Salazar 2008). This understory may provide habitat and other

73
resources to bird and other wildlife species (Carnus et al. 2006; Butler et al. 2008). For

the current study, whereas all T. amazonia plantations had understory vegetation, eight

out of ten T. grandis plantations lacked this vegetation strata because of intensive

silviculture management. Bird abundance and species richness was higher in the native T.

amazonia (1501 birds, 123 species) than in the exotic T. grandis (1278 birds, 104

species).

For bird species, several studies have compared bird diversity in natural forests

and tree plantations. In Kenya, it was found that species richness values were statistically

higher in primary forests than in monoculture tree plantations, but these were not

statistically different between primary forests and mixed-tree plantations (Farwig et al.

2008). In the north-eastern Brazilian Amazonia, species richness of primary forests was

higher than Eucalyptus plantations, with understory insectivores and canopy frugivores

being the main primary forest species absent from tree plantations (Barlow et al. 2007). A

similar pattern with the frugivorous species was found when comparing young Tectona

grandis (teak) plantations in Panama with native forest fragments (Perla et al. 2002).

Frugivorous species were found in small and large forest fragments, but were absent in

teak plantations. Despite these differences in species composition between tree

plantations and primary forests, when tree plantations can replace other human-modified

ecosystems (e.g. degraded pastures) they will almost always support a greater native

biodiversity (Brockerhoff et al. 2008).

74
Agrosilvopastoral

According to recent statistics, pastures and agrosilvopastoral land represent 77%

of the total 500 million ha of agricultural land in the Neotropics (Amezquita et al. 2005).

About 30% of these pastures are on poor, acidic soils (Montagnini 2008), as is the case in

the present study. Agrosilvopastoral systems that involve the combination of trees with

pastures and livestock offer an alternative set of cattle production systems. These systems

are more complex than grass monocultures and are classified based on the functions and

configuration or structure of trees within the system; examples are dispersed trees in

pastures, live fences in pastures, fodder banks, tree alley pasture systems, and pastures

with windbreaks (Pezo and Ibrahim 1999). Because of their increased complexity relative

to grass monoculture systems, agrosilvopastoral practices also have important benefits for

biodiversity (Harvey et al. 2005; 2006; 2008; Francesconi et al. 2010).

Many tropical pastures contain isolated trees that may be remnants of the original

forest. They are conserved by farmers for their shade for animals and humans and as

sources of firewood, timber and fruit. These trees and shrubs may be important in

attracting birds, in comparison with treeless grass monocultures. Crown size and shape,

tree height, fruit production and other characteristics may influence the ability of trees to

attract birds (Slocum and Horvitz 2000; Slocum 2001). Generally, it is thought that birds

prefer taller trees as perches to have a better view of the surroundings and to avert

potential predators. On the other hand, results of a recent study in the Pacific region of

Costa Rica suggested that crown diameter was more important than height of trees in

attracting birds (Slocum and Horvitz 2000).

75
As suggested above, a combination of several characteristics may determine the

role of each tree species in attracting birds to trees in agrosilvopastoral systems. Distance

to forest patches and position in the matrix can also have an important influence. For

example, to evaluate the contribution of living fences to improving the connectivity of the

agricultural matrix, Francesconi et al. (2010) examined bird species composition (forest

specialists, open-area specialists, and generalist species) that use living fences as habitat

in Esparza, in the Pacific lowlands of Costa Rica. Bird species composition changed as a

function of distance to the forest patch; yet species richness, number of individual birds,

and Shannon Diversity indices were similar between forest interiors (control) and living

fences. Their results suggest that living fences near forest patches provide habitats to

many bird species including forest specialists. However, fence structure and composition

significantly influenced usage by birds. The authors concluded that the presence of

diverse native tree species in fences and increased vegetative cover may counteract the

effect of distance to the forest patch, promoting greater bird species diversity in living

fences and in the landscape (Francesconi et al. 2010).

As seen, the specific types of agrosilvopastoral practices adopted by farmers are

important for the conservation of biodiversity (Enriquez et al. 2007; Saenz et al. 2007). In

a long term project in landscapes dominated by cattle in Esparza (Costa Rica), Matiguas

(Nicaragua), and Quindio (Colombia), intensive monitoring of birds in different land use

systems over four years showed that the agrosilvopastoral practices with high tree

densities in pastures and multi-strata or permanent live fences had significantly higher

abundance and species richness of birds than degraded and grass monoculture pastures,

with comparable values to those of forested vegetation (Ibrahim et al. 2010). In their

76
study, Ibrahim et al. (2010) reported that 111 bird species were observed in the landscape

of Esparza, Costa Rica, 170 species in Quindio, Colombia, and 154 species in Matiguas,

Nicaragua. Of these, a total of 60.5%, 54% and 64% of the species inventoried were

dependent on the forest in Costa Rica, Colombia, and Nicaragua, respectively. Likewise,

in a fragmented agricultural landscape in Cañas, Costa Rica, Cardenas et al. (2003)

showed that the agrosilvopastoral systems with high tree densities and permanent live

fences (multi-strata fences) had more than 40 bird species, whereas grass monoculture

pastures had 28 bird species. For the current study, agrosilvopastoral systems had one of

the highest species richness values in the corridor, and they also shared 75, 78, and 110

bird species with biological reserves, wildlife refuges, and forest edges, respectively.

However, only 34 forest-dependent species were found in these habitats, representing

20% of the total. This percentage is low in comparison to the values showed above from

other regions of the Neotropics.

Homegardens

The homegardens, which provide the household with a basic food source as well

as high value products to generate cash, are important in the tropics and are often used as

tools in development projects that promote food security, especially in the poorest areas

(FAO 2001; Montagnini 2006). In several regions of Costa Rica, homegardens are

important for supplying food (Zaldivar et al. 2002); they also serve as a buffer in times of

harvest failure or economic depression (Price 1989).

Homegardens may have positive effects on biodiversity because they can serve as

local refuges for plants and animals that otherwise may be threatened by human or

77
natural disturbances (Montagnini 2006). For example, Griffith (2000) reported that

during the 1998 fires in Petén, Guatemala, homegardens and other agroforestry systems

may have served as critical refuges during a habitat bottleneck for many forest species.

Apparently, agroforestry farms attracted birds by virtue of their complex structure –

similar to that of intact forest patches – and they harbor insects, provide nesting sites, and

offer protection from predators (Griffith 2000). Birds were also attracted by the cultivated

fruit trees, which may have provided some of the only food sources in the region after

fire destroyed most of the surrounding vegetation. Homegardens tend to attract many bird

species of different guilds (Scales and Marsden 2008). For the present study,

homegardens were one of the land uses with the highest accumulated number of bird

species (185 species). They shared 91, 92, and 126 species with wildlife refuges,

biological reserves, and forest edges, respectively, having the second largest number of

forest dependent species (51 species). However, they are disappearing as local people are

selling their properties to developers, who usually replace the complex structure of

native/exotic plants with a simpler one based on exotic species. Also, the area under

construction has increased, especially because most of the new residential areas request

commodities such as swimming pools.

Oil palm

As a result of the rising demand for vegetable oils and biofuels, oil palm (Elaeis

guineensis) is one of the world’s most rapidly increasing crops (Fitzherbert et al. 2008),

becoming a major threat to tropical biodiversity (Turner et al. 2008; Koh and Wilcove

2008). At present, oil palm is grown across more than 13.5 million ha of tropical regions

78
(Fitzherbert et al. 2008). In Costa Rica, the oil palm industry is relatively small, but is

one of the oldest in tropical America. The first commercial plantation was established in

1944. In 2006, the industry covered about 47,807 ha, mostly established on the central

and southern parts of the Pacific coast (96%) (Escobar and Peralta 2007).

According to Fitzherbert et al. (2008), there were only 13 published scientific

papers comparing wildlife diversity in oil palm plantations to that in forests from 1970 to

2006. Overall, oil palm plantations support many fewer species than do forests and often

fewer than other tree crops as well (Fitzherbert et al. 2008). Moreover, species

composition is different between these two habitat types. While most species with

specialized diets and microhabitat were absent from oil plantations, plantation

assemblages were dominated by a few abundant generalists, open-area species, invasive

species and pests (Aratrakorn et al. 2006; Peh et al. 2006; Chey et al. 2006; Fitzherbert et

al. 2008). Oil palm plantations also have lower species richness than do other agricultural

types (Fitzherbert et al. 2008). For the present study, and with the exception of the

assessed villages, oil palm plantations had the lowest diversity values, sharing only

approximately 50 species with the forested habitats, and registering only 22 forest-

specialist species.

As a result of the low conservation value found in oil palm plantations, several

authors have suggested two main approaches for enhancing biodiversity conservation at

the landscape level. The most commonly cited is to preserve as much of the remaining

natural forests by either protecting forest in reserves, buffer zones around plantations, or

forest fragments within the plantations and at the landscape level (Fitzherbert et al. 2008;

Koh 2008; Turner et al. 2008). Conversely, other researchers advocate for the

79
implementation of traditional agroforestry practices to create a more heterogeneous

landscape benefiting both biodiversity and rural communities (Bhagwat and Willis 2008;

Koh et al. 2009). Claims of using agroforestry systems focus on the oil palm plantations

lower species richness values for some taxa in comparison with agroforestry systems

based on rubber plantations (Hevea brasiliensis), cocoa (Theobroma cacao), and coffee

(Coffea canephora) in Southeast Asia (Bhagwat and Willis 2008; Koh et al. 2009). Most

of the sampling points for this study had more than just palm vegetation including living

fences, and remnant trees, among others. In fact, more than 43% of birds found in the oil

palm plantations were registered when utilizing such microhabitats (Chapter 4).

Urbanization

Forest loss with accompanying urbanization is often permanent as forests are

replaced by concrete structures or surfaces. The remaining forest patches are usually

isolated and too small to maintain viable populations of forest-dependent wildlife species

(Er et al. 2005). The effect of urbanization on wildlife conservation can be immense;

however, our understanding is still rudimentary according to some reviews (McKinney

2002; Chace and Walsh 2006). For birds, urban development can affect native species in

many ways because human-influenced changes in the environment often result in

alterations to multiple elements of their habitats (McCaffrey 2009). Therefore, because

birds respond to vegetation composition and structure, urban areas that retain native

vegetation features retain more native species than those that do not (Chace and Walsh

2009).

80
How an individual species is affected by these changes depends on both the

specific habitat features they require as well as the scale at which they respond to habitat

changes (McCaffrey 09). Marzluff and Ewing (2001) and Chace and Walsh (2006)

summarize the factors determining which species can coexist with human settlement as

follows: (1) the presence and patch size of remnant (native) vegetation (Catterall et al.

1991; McKinney 2002; Er et al. 2005; Suarez-Rubio and Thomlinson 2009), (2)

competition with exotic species (Major et al. 1996; McKinney 2002; Er et al. 2005), (3)

non-native predators (Churcher and Lawton 1987; Paton 1990), (4) the structure and

floristic attributes of planted vegetation (Suarez-Rubio and Thomlinson 2009), (5)

supplementary feeding by humans (Brittingham 1990; Major et al. 1996), (6) obstruction

of traditional migratory and dispersal routes and increasing the dangers of dispersal

(Marzluff and Ewing 2001), and (7) residual pesticides (Major et al. 1996).

Overall, as the urbanization processes increase, there is an increase in avian

biomass and induced community homogenization, but a reduction in richness (Chance

and Walsh 2006; Devictor et al. 2007). Some studies have shown that the urbanization

matrix is correlated negatively with native species (Er et al 2005; Chace and Walsh 2006;

Suarez-Rubio and Thomlinson 2009), especially endemic species (Suarez-Rubio and

Thomlinson 2009), and forest-specialist species (Er et al. 2005), but positively with

introduced species (Suarez-Rubio and Thomlinson 2009). Urbanization tends to select for

omnivorous, granivorous, and cavity nesting species (Chace and Walsh 2006). Villages

and residential tourism projects were the two land-use types where cement and concrete

were part of the landscape. However, residential tourism projects tended to keep larger

forest cover around the houses in relation to the selected 20 sampling points in villages

81
and that may explain why the former had 33 forest-specialist species and the latter only

19 species (the lowest of all land-use types). Also, shared species with forested habitats

were higher for residential tourism projects (70 - 101 species) than for villages (52 – 78

species). Land-use change from forested habitats to any residential project should be

avoided in areas where infrastructure may limit the connectivity among forest reserves.

Conclusions: Implications for land-use planning

This study was carried out in a high biodiverse human-modified biological

corridor that is under threat because of residential and tourism development, and whose

main goal is to provide connectivity to the forested reserves. Therefore, management of

the different land-use types as well as their components may have positive or negative

biodiversity implications and should be taken into consideration in land-use planning.

It is important to stress that biodiversity conservation should always include

primary and old-secondary forests (e.g. those forests located in wildlife refuges,

biological reserves, or isolated forest fragments) because the majority of bird species

utilize these habitats the most. Moreover, these are the most important habitat types for

forest-dependent wildlife at the landscape level, and these species are usually more

susceptible to fragmentation and land-use change. However, the results of this research

also show that the matrix around these forests, especially young secondary forests,

homegardens, agrosilvopastoral systems, and tree plantations, are important in expanding

the potential habitat for many bird species in a biological corridor, including both forest

and non-forest species.

82
Agroforestry systems such as agrosilvopastoral systems and homegardens are

diverse habitats that, if managed in the proper way, may increase the current contribution

of the PTBC and other fragmented habitats to wildlife conservation. Adding native tree

species, especially fruit trees, in agricultural systems adjacent to forested areas may add

conservation value to these habitat types, attracting endangered bird species such as Ara

macaw and other forest-dependent bird species (Chapter 4 and 5).

According to the data in this study, it may even be possible to implement

agrosilvopastoral systems that are compatible with production objectives and biodiversity

conservation. Good farm planning is needed, including a mosaic of land uses that are

compatible with both the conservation of biodiversity and production objectives (Saenz et

al. 2007; Harvey et al. 2008). For example, cattle farms could incorporate land uses

which include establishment of fodder banks, multi-strata live fences, and pastures with

high tree cover or density, as well as riparian and secondary forest (Ibahim et al. 2010).

Planting native tree species, such as Terminalia amazonia and other native tree

species of interest in Costa Rica and elsewhere in the Neotropics, could be given priority

to serve biodiversity and economic objectives of humans inhabiting the corridor.

Finally, forest fragmentation, unplanned urbanization, monocultures, and the

introduction of exotic plant species could be avoided in biological corridors in order to

avoid jeopardizing native biodiversity. One example of these monocultures that could be

avoided is oil palm plantations. Even though more than 100 species were found in the oil

palm plantations, their species richness value was one of the lowest of all evaluated

habitats. Furthermore, the worldwide expansion of this type of plantation is cited as a

major threat to tropical biodiversity.

83
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Table 3.1. Abundance, species richness, and diversity of birds registered in ten land-
use types in the Path of the Tapir Biological Corridor, Costa Rica

Habitat Type Abundance Species Richness Shannon


(n/census) (species/census) Index
Homegardens 574 (13.2)a 89 (3.3)a 3.88 (0.04)ab
Agrosilvopastoral Systems 533 (13.8)a 82 (2.9)ab 3.84 (0.04)b
Villages 500 (15.9)a 57 (1.9)c 3.35 (0.02)d
Oil Palm 361 (9.2)b 55 (1.6)c 3.45 (0.05)d
Forest Fallows 380 (15.2)c 84 (3.2)a 3.93 (0.05)ab
Residential Tourism 349 (16.1)bc 64 (2.6)bc 3.70 (0.04)c
Forest Edges 296 (17.1)c 83 (3.2)ab 3.96 (0.04)a
Wildlife Refuges 269 (14.2)cd 71 (2.6)b 3.83 (0.02)b
Biological Reserves 250 (12.8)cd 69 (2.4)b 3.84 (0.03)ab
Tree Plantations 231 (15.5)d 62 (2.6)bc 3.77 (0.05)bc

Data represents means per census (N = 12) and standard errors. Different letters within same column
indicate differences across land use types

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Table 3.2. Sorensen similarity index (top values) and shared species (bottom values)

of ten land-use types in the Path of the Tapir Biological Corridor

Sorensen Index
BR FE FF HG OP ASP WR RT TP VI
BR 0.756 0.628 0.524 0.373 0.444 0.825 0.505 0.619 0.385
FE 135 0.753 0.663 0.486 0.593 0.754 0.62 0.729 0.489
FF 109 143 0.762 0.58 0.704 0.609 0.715 0.775 0.583
HG 91 126 141 0.671 0.792 0.523 0.772 0.757 0.699
OP 53 77 89 103 0.711 0.358 0.735 0.652 0.74
ASP 75 110 127 143 106 0.46 0.736 0.691 0.7
WR 134 135 106 91 51 78 0.476 0.624 0.362
RT 74 101 113 122 93 113 70 0.76 0.729
TP 96 125 129 126 88 112 97 106 0.647
VI 55 78 90 108 91 105 52 93 88
Number of Shared Species

BR = Biological Reserves, FE = Forest Edges, FF = Forest Fallows, HG = Homegardens, OP = Oil palm,

ASP = Agrosilvopastoral systems, WR = Wildlife Refuges, RT = Residential Tourism Projects, TP = Tree

Plantations, VI = Villages.

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Figure 3.1. Location of the Path of the Tapir Biological Corridor, Costa Rica.

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Figure 3.2. Accumulated number of bird species found in ten different habitat types

in the Path of the Tapir Biological Corridor, Costa Rica.

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Figure 3.3. Relative abundance of the five more abundant bird families per land-use

type in the Path of the Tapir Biological Corridor, Costa Rica

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Figure 3.4. Accumulated expected number of bird species (2-year data) in ten

habitat types in the Path of the Tapir Biological Corridor, Costa Rica.

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R P P G T
VI W BR FE TP O AS H FF R

-400
Similarity

-800

1200

0 1 2 3 4 5 6 7 8 9 10
Land-use Type

Figure 3.5. Similarity of bird assemblages across ten habitat types in the Path of the

Tapir Biological Corridor, Costa Rica

FE = Forest Edges, FF = Forest Fallows, BR = Biological Reserves, WR = Wildlife Refuges, HG =


Homegardens, TP = Tree Plantations, ASP = Agrosilvopastoral systems, RT = Residential Tourism
Projects, OP = Oil palm, VI = Villages.

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Chapter 4

Response of Bird Guilds to Ten Different Land-use Types in a Human-Modified


Biological Corridor, Costa Rica: Conservation Implications

Abstract

Many bird species are important because they provide important ecosystem

services such as pest control, pollination, and seed dispersal. This chapter aims to

describe the main bird guilds found in the Path of the Tapir Biological Corridor (PTBC)

and how they contribute to the corridor’s conservation goals. A total of 200 points were

monitored for a period of 400 hours along a two-year period, including ten land-use

types: wildlife refuges, biological reserves, forest edges, forest fallows, residential

tourism projects, villages, tree plantations, homegardens, oil palm plantations, and

agrosilvopastoral systems.

At each point, aside from identifying each bird seen, the microhabitat where they

were seen was recorded (e.g. tree, shrub/bush, palm, human infrastructure, etc) as well as

bird activity (e.g. foraging, perching, just moving). Relative to feeding guilds, of the 301

species and 43,911 birds included in this assessment, 53.8% of species were classified as

insectivores, 21.2% frugivores, 9% nectarivores, and carnivores and granivores 8% each

one. On the other hand, classification of birds by habitat preferences depicted that 44.5%

of total species were forest specialist, 38.9% forest generalist, and 16.6% open area

species. Relative abundance of species did not present statistical differences across the

ten land-use types for feeding guilds (G = 5.14, df = 5, p = 0.398), but it did for habitat

guilds (G = 8.372, df = 3, p = 0.039). However, statistical differences were found for

average number of species and abundance for both guild assemblages across the ten land-

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use types (p < 0.05). As anticipated, for forest-dependent species, wildlife refuges,

biological reserves, and forest edges were the best habitat. However, tree plantations,

homegardens, and forest fallows were also important habitats for this group. The lowest

number of forest specialist species was found in oil palm plantations. Open-area species

were more commonly found in agrosilvopastoral systems, villages, homegardens, and oil

palm plantations. For the bird assemblages that provide specific environmental services,

the understory insectivores and large-seed disperers are the groups that may be of further

conservation priority because they are more sensitive to disturbances. Moreover, aside

from protection of forests, management of more complex homegardens and silvopastoral

systems, forest fallows, and native tree plantations can contribute to the protection of bird

species of concern and therefore the environmental services they provide to the

environment.

Introduction

Because of the concerns about the effects of habitat loss and fragmentation on

wildlife conservation, there have been an increasing number of studies on single species

or assemblages in fragmented landscapes throughout the world (Laurance and

Bierregaard 1997; Bennett 2003). However, most of these studies have focused on the

fragments themselves, ignoring species' distribution in surrounding sites such as

agricultural or other human-dominated areas (Ricketts et al. 2000, Chazdon et al. 2009).

Overall, it has been stated that bird species respond differently to disturbances and that

species’ ecological traits (body size, local population size, and geographic range size) and

evolutionary relationships may influence responses in some guilds (Gray et al. 2007).

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For instance, Gray et al. (2007), based on 25 studies and 1178 bird species in Asia and

the Neotropics, found that after disturbances granivores population increased and

frugivores and insectivores declined in both Asia and Neotropical regions.

Aside from the impact of disturbances on wildlife species, there is a general

concern regarding the effect that disturbances can have on functional diversity, food web

interactions, and ecosystems functioning, especially in human-modified landscapes in the

tropics where there is little known (Petit and Petit 2003; Farwig et al. 2008; Tscharntke et

al. 2008). Therefore, for conservation planning of buffer zones, biological corridors, and

other human-modified landscapes, studies of habitat utilization by wildlife species

assemblages are needed to identify key habitats, foraging and nesting sites, and dispersal

routes of animal guilds in planning conservation units (Chazdon et al. 2009). At the

landscape level, it is also important to determine the presence of species in these habitats

that provide ecological services (Tscharntke et al. 2008; Chazdon et al. 2009). For

instance, many bird species are important because they often provide important

ecosystem services such as pest control, pollination, and seed dispersal (Sekercioglu

2006; Tscharntke et al. 2008).

This chapter aims to describe the main bird assemblages found in the human-

modified Path of the Tapir Biological Corridor and how these assemblages affect

conservation goals. These bird assemblages are based on bird diet as well as preferred

habitat. First, there will be a description of bird species distributions based on their

different feeding and habitat guilds in the PTBC. Second, how bird guilds utilized the ten

land-use types is explored in detail, and finally how presence or absent of specific guilds

may affect ecosystem functions and vegetation composition is explained.

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Methods

Study site description, land-use types assessed, and data collection

For this chapter, the same ten habitat types and their corresponding 20 point

counts per land-use type described in Chapter 3 were used: forest edges, forest fallows,

wildlife refuges, biological refuges, tree plantations, villages, oil palm plantations,

residential tourism projects, agrosilvopastoral systems, and homegardens.

When conducting bird surveys, the bird activity at the time of observation was

recorded (e.g. foraging, nesting, perching, or just moving), as well as the microhabitat

where they were found. Microhabitat categories varied from trees, shrub, bush, palm,

grass/ground, to human infrastructure (e.g building, house, fence, and utility wire). The

microhabitat’s height where birds were observed was also estimated.

Bird guilds

For the present analysis, birds were classified by habitat and feeding preferences.

Bird species were classified in three habitat guilds: forest specialist species, forest

generalist species, and open area species (Stiles and Skutch 1989; Garrigues and Dean

2007). Forest specialists are the species that mostly utilize closed-canopy forests. Forest

species were also classified as canopy and understory forest species. Canopy birds were

defined as the species that frequent middle and upper levels of close-canopy forests

whereas understory birds were defined as the species that spend most of their time in

understory vegetation or on the ground. Both understory and canopy birds can be found

in closed-canopy, primary and old-secondary forests. Forest generalist species can

occupy closed-canopy forests as well as forest edges and clearings. Open-area species are

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not found in forests; they usually frequent areas where trees may be present, but not

necessarily.

Bird species were also classified based on their primary diet preference as

frugivores (e.g. fleshy fruits), nectarivores (nectar), carnivores (large arthropods and

vertebrate prey), granivores (seed and nuts), and insectivores (small arthropods),

following Stiles and Skutch (1989) and Garrigues and Dean (2007).

Data analysis

This chapter’s analysis did not include nocturnal species, or species commonly

found in wetland ecosystems, or swifts and swallows because I did not sample wetlands

and or conduct nocturnal surveys. Moreover, most literature excludes these species when

guild analysis is included (e.g. Hughes et al. 2002)

A one-way ANOVA was used to compare mean number of species and mean

abundance across land-use types. The means were estimated based on values for each of

the 12 censuses conducted. For habitat and feeding guilds, a log-likelihood G statistic

was computed to compare the overall guild structure of bird communities among all

habitats, represented as the number of species in different guilds (Petit and Petit 2003).

The nonparametric test Kruskal-Wallis was used to compare the incidence (percentage of

species) and relative abundance (percentage of birds) for each guild among habitat types.

Krustal-Wallis was also performed to compare bird activity when recorded (the

percentage of birds per activity) as well as to compare the structure where birds were

observed (the percentage of birds per tree/shrub/bush) among the ten different land-use

types. Non-metric multidimensional scaling (NMDS) were performed to see the

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relationship between canopy and understory forest species and land-use types. All

statistical analyses were conducted in PAST v 1.95 (Hammer et al. 2001) and R statistical

software.

Results

Habitat guilds

For the current analysis, 301 species and 43,911 individuals were taken into

account. Of these, 44.5 % were classified as forest specialists, 38.9% as forest generalists,

and 16.6 % as open area specialists. Comparing the total accumulated number of bird

species, the distribution of habitat guild members differed significantly across the ten

land-use types (G = 8.372, df = 3, p = 0.039; Figure 4.1) consistent with the predicted

habitat requirements of guild members. Guild assemblages shifted gradually from a

predominance of forest specialists and just a few open area specialists in forested habitats

to a higher proportion of open area species and few forests specialist in open area land-

use types such as villages and oil palm plantations (Figure 4.1). Analysis of variance also

depicted statistical differences for species richness and abundance across the ten habitat

types (p < 0.05; Table 4.1). Wildlife refuges, biological reserves, and forest edges had the

highest abundance and species richness values for forest specialist species and also the

lowest for open area specialists, as anticipated. Concentration of species and abundance

of understory and canopy forest specialist were also different across the ten habitat types

(Figure 4.2; 4.3). The differences among forested habitats and open area habitats were

better identified by understory specialist than by canopy specialist. Many canopy species

can move more easily to land-use types other than forests in search of food because of

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dispersal abilities (e.g. parrots & parakeets). Forest generalist species were more

commonly found in homegardens, followed by forest fallows and agrosilvopastoral

systems. Open area species were more commonly found in agrosilvopastoral systems,

villages, homegardens, and oil palm plantations.

Feeding Guilds

In general, of the 301 bird species included in this analysis, 53.8 % corresponded

to insectivorous species, 21.2 % to frugivores, 9% nectarivores, and 8% each to

carnivores and granivores. Contrary to the findings of habitat guilds, when comparing the

total accumulated number of bird species, distribution of feeding guild members did not

differ significantly across the ten land-use types (G = 5.14, df = 5, p = 0.398; Figure 4.4).

However, there were statistical differences across the ten habitat types for species

richness and abundance when compared at the census level (p < 0.05; Table 4.4).

Insectivorous species not only had the most species, but also had the most

individuals registered (40.4%). The majority of insectivorous species were recorded at

forest edges and forest fallows, followed by wildlife refuges, biological reserves, and

agrosilvopastoral systems. The most important species in terms of abundance were house

wren (Troglodytes aedon) great kiskadee (Pitangus sulphuratus), tropical kingbird

(Tyrannus melancholicus), red-crowned woodpecker (Melanerpes rubricapillus), and

chestnut-backed antbird (Myrmeciza exsul), all together representing 32.5 % of the total

birds for this guild. The former four species were observed more in open habitats while

the antbird was recorded mostly in forested habitats.

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Although frugivores had only 21.2% of the total number of species, they

encompassed 36.9 % of the total number of registered birds. They were more commonly

found in homegardens and forest edges and the most common species were cherries

tanager (Ramphocelus costaricensis), blue-gray tanager (Thraupis episcopus), orange-

chinned parakeet (Brotegeris jugularis), palm tanager (Thraupis palmarum), and

chestnut-mandibled toucan (Ramphastos swainsonii). These five species represent almost

36% of total frugivore sightings. Aside from the toucan, all species did not visit closed-

canopy forests. Oil palm plantations had a statistically lower species richness and

abundance values across the 10 land-use types (p < 0.05).

Granivores represented 17% of total records for this study. As expected, average

abundance and species richness were highest for open habitats such as agrosilvopastoral

systems, oil palm plantations (e.g. young plantations), homegardens, and villages. On the

contrary, the lowest numbers were found in the forested land-use types. The most

commonly found species were great-tailed grackle (Quiscalus mexicanus), variable

seedeater (Sporophila americana), blue-black grassquit (Volantinia jacarina), ruddy-

ground dove (Columbina talpacoti), and white-tipped dove (Leptotila verreauxi),

representing 81.7% of the registered granivores. Quiscalus mexicanus is considered an

invasive species of open areas.

Nectarivores and carnivores comprised only 3.8% and 1.9% of the birds,

respectively. While nectarivores tended to be more commonly found in homegardens and

forest edges, carnivores were more commonly encountered in agrosilvopastoral systems,

villages, and oil palm plantations. Blue-throated goldentail (Hylocharis eliciae), rufous-

tailed hummingbird (Amazilia tzacatl), bananaquit (Coereba flaveola), long-billed hermit

106
(Phaethornis logirostris), and purple-crowned fairy (Heliothryx barroti) were the most

abundant nectarivorous species (64.0% of all nectarivores); and roadside hawk (Buteo

magnirostris), black vulture (Coragyps atratus), turkey vulture (Cathartes aura), yellow-

headed caracara (Milvago chimachima), and laughing falcon (Herpetotheres cachinnans)

were the most commonly recorded carnivores, representing 83.9% of all birds in this

guild.

Resource use

Overall, it was estimated that the activity of a particular bird was not independent

of the land-use type where found (X2 = 1594.1; df = 27; p < 0.001). Moreover, birds were

recorded foraging more than any of the other activities (perching, moving, or nesting) in

the ten different land-use types (Figure 4.5). Of all species, 263 species (87.4%) were

registered foraging at least once, with forest fallows (154 species), homegardens (145

species), and forest edges (144 species) being the most visited habitats. In contrast, only

51 species were registered nesting, preferring homegardens (21 out of 51 species) and

villages (16 out of 51 species). Great kiskadee was observed nesting 41 times, social

flycatcher (Myiozetetes similis) 21 times, gray-capped flycatcher (Myiozetetes

granadensis) 13 times, and the yellow-throated euphonia (Euphonia hirundinacea),

golden-hooded tanager (Tangara larvata), and streaked flycatcher (Myiodynastes

maculates) 10 times each.

Finally, the bird preference by microhabitat (e.g. trees, shrubs/bush, ground,

human infrastructure) was assessed. It was found that microhabitat used by birds and

land-use are not independent (X2 = 21095; df = 36; p = 0.000; Figure 4.6). In general,

107
with the exception of oil palm plantations, more than 65% of the individuals were

observed in trees, a small percentage were also recorded in shrub/bush combinations and

the least were observed in the ground/grass and human-infrastructure (e.g. utility wires,

fences, buildings). It is important to highlight that more than 43 % of sightings in oil

palm plantations were recorded in plants other than the palms, highlighting the

importance of other vegetation in large-scale monocultures. Remnant trees and living

fences were a part of these monocultures, as well as grassy/bushy areas in younger stages

of the palm plantations.

Discussion

Habitat guilds

Conservation of bird guilds in human-dominated landscapes depends on many

factors, including the configuration of the matrix around forested areas as well as the

adaptability of many of these species assemblages to changes at the micro and macro

level (Sodhi et al. 2004; 2008; Brockerhoff et al. 2008). The general concept that the

human-modified landscapes are very important for the conservation of open-area and

forest-generalist bird species was confirmed in this study. However, it was found that 70

out of 134 forest-dependent species were also utilizing these habitats. Understanding the

persistence mechanism of tropical forest species in human-modified landscapes is

therefore a fundamental challenge of tropical ecology and conservation, especially

because of the low adaptability of many of these species to disturbances (Sodhi et al.

2004; Sekercioglu et al. 2006).

108
Several studies have shown that some of these human-modified land-use types

can contribute to the conservation of a portion of forest specialists (Petit and Petit 2003;

Farwing et al. 2008). For instance, in western Kenya, Farwing et al. (2008) did not find

statistical differences in the number of forest specialist species between natural forests

and native mixed and pure plantations. All of these land-use types had a higher number of

forest specialists than exotic monocultures in the same region (Farwing et al. 2008). In

the current study, for forest bird species, forested habitats were statistically more diverse

and more abundant than any other human-modified land-use type. However, 67, 55, and

51 forest specialist species utilized forest fallows, tree plantations, and homegardens as

alternative habitat, respectively. From the conservation point of view, this is positive

because it indicates that not all forest species are totally restricted to forested habitats,

increasing availability of suitable habitat, especially for connectivity purposes.

Forest fallows or secondary forests have been mentioned as an alternative habitat

for forest species (Dunn 2004; Waltert et al. 2004; 2005; Chazdon et al. 2009). In

Uganda, songbird community composition and richness of forest bird species were

similar between intact, mature forest and 13-year old regeneration forest (Naidoo 2004).

However, some studies have found that secondary forests and exotic tree plantations can

only hold a few forest species compared to primary forests (Zurita et al. 2006; Barlow et

al. 2007), contradicting the conservation values of secondary forests described in other

studies. Regardless of these numbers, both tree plantations and secondary forests may be

more suitable habitat than degraded traditional pasturelands. For instance, cattle pastures

left fallow for less than two years supported more than twice as many total species as

actively grazed pastures in Panama (Petit et al. 1999). In Colombia, tree plantations also

109
had higher bird species richness than other more intense production systems such as

pasture lands (Mendoza et al. 2007).

For the present study, tree plantations also had statistical differences from the

native and the exotic species assessed as a part of this study. For instance, twice as many

forest specialist species utilized T. amazonia plantations (native - 52 species and 684

individuals) than T. grandis plantations (exotic - 26 species and 100 individuals).

According to Brockerhoff et al. (2008), the extent of the difference between natural forest

and tree plantations varies considerably across the range of management intensities and

the degree to which plantations deviate from the tree species composition and structure of

natural forests in the same region. Natural regeneration growing beneath the canopy of

most T. amazonia plantations may provide different micro-habitat conditions than the

absence of understory under T. grandis plantations because of different management

regimes. Only three out of 55 forest specialist species found in the tree plantations were

solely recorded in T. grandis and not in T. amazonia: olivaceous piculet (Picummus

olivaceus -1 bird), yellow-bellied flycatcher (Empidonax flaviventris - 3 birds), and

scarlet macaw (Scarlet macao - 2 birds).

As for native tree plantations, complex agroforestry systems such as homegardens

and some types of agrosilvopastoral systems are more supportive of forest species than

mono-crop systems (McNeeley and Schroth 2006; Scales and Marsden 2008). However,

as for secondary forests and tree plantations, the presence of forest-dependent species in

agroforestry systems depends on several factors; and most of the time agroforestry

systems have been cited as having a low number of species from this guild compared to

primary forests (Scales and Marsden 2008).

110
For the current study, it is interesting to note that a few forest specialists were

found even in highly human-impacted habitats such as villages and residential tourism

projects as well as large-scale monocultures such as the oil palm plantations. However,

because development is an unplanned ongoing process in the region (Redondo-Brenes

and Villalobos 2008), response of bird species composition and abundance may change

in the coming years as urbanization spreads along the corridor. For now, even the

endangered scarlet macaw can be seen in a few of the villages and homegardens,

especially southern ones where macaws feed on several tree species around human

settlements (See Chapter 5). Contrary to these findings in the PTBC in Panama, Petit and

Petit (2003) did not report any forest specialist species utilizing fallow pastures, pine

plantations, sugar cane, grazed pastures, villages, and rice paddies.

Overall, data from the corridor landscape matrix for bird species seems to present

promising numbers in comparison to some other studies in the tropics, especially with

regard to the utilization of these human-modified habitats by forest species. However,

because distance from primary forest was not taken into account and many of the

sampling points were close to them, this factor may favor the presence of more forest-

dependent species in the human-modified matrix (Barlow et al. 2007). Some of the

forest-specialist species recorded in this study frequently utilizing the human-modified

landscape were the chestnut-mandibled toucan, red-lored parrot (Amazona autumnalis),

fiery-billed aracari (Pteroglossus frantzii), short-billed pigeon, and cocoa woodcreeper

(Xiphorhynchus susurrans), great crested flycatcher (Myisrchus crinitus), mealy parrot

(Amazona farinose), and scarlet macaw. Each species was observed more than 100 times

over the 12 censuses in the 2-year period of this study. With the exception of the fiery-

111
billed aracari in oil palm plantations, cocoa woodcreeper in villages, and scarlet macaws

in oil palm, agrosilvopastoral systems, and residential tourism projects, all other highly

abundant species were found in all six human-modified habitats.

Bird feeding guilds and environmental services

In most rain forests, birds are the single most important group of seed dispersal

agents (Primack and Corlett 2005), and the fate of the seed – and thus the success of seed

dispersal - depends critically on how the frugivorous animals select and process the fruits,

and what it does afterwards (Primack and Corlett 2005). For instance, it was estimated

that 90% of seed dispersal agents for 336 tree species in ten tropical rain forests of

northern Costa Rica were animals (Chazdon et al. 2003). Guindon (1997), studying seed

dispersal of cloud forests in Costa Rica, also reported that 80% of 225 tree species in his

study site depended on vertebrates for their dispersal with most (63%) primarily by birds.

Several studies in the tropics have shown that the loss of frugivores in forests can have

significant impacts on forest structure and composition (Guindon 1997; Gross-Camp et

al. 2009; Moran et al. 2009). For instance, change in the composition of the frugivores

assemblage in fragmented subtropical Australian forests has decreased the dispersal of

12% of the native plants species; and populations of these plants have substantially

reduced in the region studied (Moran et al. 2009). In addition, lack of bird dispersers for

the endemic tree Leptonychia usambarensis (Sterculiaceae) was the main factor

associated with seedlings and saplings being more aggregated around mother trees in

fragmented forests than in continuous forests in Tanzania (Cordeiro and Howe 2003),

increasing predation and therefore mortality.

112
In the PTBC, frugivorous species composition changed across the ten different

habitat types, but abundance of frugivores was similar across most land-use types, except

oil palm plantations where it was lowest (Figure 4.4, Table 4.2). For conservation

purposes, this similarity is important because bird abundance rather than species richness

has been mentioned to be the main factor that drives seed dispersal in human-modified

landscapes (Pejchar et al. 2008). Moreover, in fragmented forests small-seeded plants

may be more resilient to forest fragmentation while large-seeded species may be more

susceptible because large-seeded species rely on a few, extinction-prone dispersers

(Guindon 1997; Cramer et al. 2007), and should be a priority for conservation. In the

PTBC, important small-seed dispersal families such as Frigillidae (euphonia), Thraupidae

(tanagers), and Pipridae (manakins) were recorded in large numbers in all habitat types.

The latter family was found mostly in forested areas, but the former two were

encountered in different land-use types.

Some general, large-seed dispersal birds such as chestnut-mandibled toucan were

registered in all ten land-use types. The other member of the Ramphastidae family, the

fiery-billed aracari, was also found in all habitats except oil palm plantations. Other

large-seed dispersers such as great curassow (Crux rubra) and crested guan (Penelope

purpurascens - both Cracidae) were totally restricted to forested habitats and both are

enlisted as endangered species (See Chapter 5). Of greater concern is the crested guan

whose observations were lower than great curassow. The Three-wattled bellbird

(Procnias tricarunculatus), an altitudinal migrant species, is another large-seed disperser

that was also restricted to forested habitats. This species is considered an important

dispersal agent, especially of the Lauraceae family in montane forests of Costa Rica

113
(Guindon 1997). The trogons (Trogodinae), also known as important middle-size seed

dispersal agents in the tropics (Primack and Corlett 2005), were found in most habitat

types, especially forests, homegardens, silvopastoral systems, and tree plantations.

Like frugivores, nectarivores have important consequences for plant population

and community dynamics (Sekercioglu et al. 2004). However, the proportion of bird

species that provide pollination services to plants in the Neotropics is lower than those

that disperse seeds (Primack and Corlett 2005). In fact, Chazdon et al. (2003) found that

only 24 out of 336 tree species in Northern Costa Rica were primarily pollinated by

hummingbirds, the main bird pollinator group in the Neotropics (Primack and Corlett

2005). Hummingbirds usually pollinated herbaceous plant species such as Heliconias and

other forest understory plants (Primack and Corlett 2005). For the current study, 27

hummingbird species were identified, favoring homegardens, forest edges and forest

fallows, where abundant numbers of flowering herbaceous plants were available.

However, it was also interesting than 47% of the time, hummingbirds were registered

foraging on trees. Flowers of tree species such as Erythrina poepiggiana, Cedrela

odorata, Bombacopsis quinatum, several species of the genus Inga sp, Cecropia sp,

several fruit trees, among others, were some of the trees hummingbirds commonly

visited.

In the tropics, the most common guild of bird species is the insectivores (Primack

and Corlett 2005). However, because of their high ecological specialization, they are

highly sensitive to fragmentation and therefore are extinction-prone (Sekercioglu et al.

2004), especially forest understory species (Rendijo 2001; Laurance et al. 2002; Lens et

al. 2002; Siegel et al. 2006; Stouffer et al. 2006; Peters et al. 2008). For the present study,

114
insectivores accounted for 53.8 % of the species registered. They were found in the ten

land-use types, with forest edges, forest fallows, biological reserves, wildlife refuges, and

homegardens being the most important land-use types for this guild. The lowest numbers

for both frugivores and nectarivores were in oil palm plantations. As mentioned above,

understory insectivores have been cited as the guild that is most affected by

fragmentation and land-use change. For the ten land-use types in this study, numbers

confirm that pattern, as more understory insectivores were restricted to forested areas (13

out of 33 - 40% of total members for this guild) than canopy insectivores (22 out of 129 -

only 17% of all members for this guild).

Insectivores feeding not only benefits natural forests (Van Bael et al. 2003), but

also important crops in tropical countries such as coffee (Kellernmann et al., 2008;

Johnson et al. 2009), cocoa (Van Bael et al. 2007), and oil palm plantations (Koh 2008)

by decreasing foliage damage by arthropods. Furthermore, insectivorous birds can benefit

human welfare by increasing total revenues from healthier crops. For instance, in

Jamaica, Kellermann et al. (2008) estimated a benefit of US $4018 (118% of the per

capita GNI for the 2004-2005 season) to four farmers from bird insectivores, which led to

healthier coffee fruits , and consequently increased value on international markets.

Another bird group that also provides benefits to the environment and humanity

are the carnivores. They are important in maintaining low rodent populations and also

have important decomposition functions (e.g. scavengers) (Primack and Corlett 2005). In

the PTBC they seem to be equally distributed, but are not abundant in species and

individuals compared to frugivores or insectivores. The largest raptors that depend on

forested areas are the ones that seemed to be under more serious threats as a result of

115
forest disappearance. However, whereas at present they can be seen in various locations

throughout the corridor, according to local residents most of them were gone because of

losing of forest cover in the 1960s and 1970s. White hawks (Leucopternis albicollis) and

King Vultures (Sarcoramphus papa) exemplify two of the species that are more

commonly found in the corridor now than 10-20 years ago.

Conclusions

In the Path of Tapir Biological Corridor, land use has changed from dense

primary forests in the 1900s to extended and degraded pasture lands in the 1960s and

1970s (Redondo-Brenes and Montagnini 2010). This was followed by the recovery of at

least 50-60% of the forest cover throughout 1990s and 2000s through natural

regeneration and establishment of tree plantations (Redondo-Brenes 2007; Redondo-

Brenes and Montagnini 2010). However, as land value has increased, a new and

uncontrolled tourism and residential development boom is jeopardizing the connectivity

of large forest fragments in most of the Pacific coast of Costa Rica (Redondo-Brenes and

Villalobos 2008). The disappearance of natural forests and consequent avian composition

shift may also affect several of the environmental services that birds provide to the

system, including pest control, seed dispersal, and pollination.

Conservation planning should focus on protecting main forest fragments within

biological corridors, limiting residential development in these areas, especially to protect

some of the most sensitive guilds such as understory insectivores and large-seed

dispersals that are only found in closed-canopy primary and old-secondary forests.

116
In addition, land-use practices that include management of more diverse

agroforestry systems, native tree plantations, and secondary forests as buffer zones or as

connectors of the already existing forest fragments should be promoted in order to

provide more suitable habitat for the forest-dependent species and open-area species.

Moreover, inclusion of more fruiting trees as part of the landscape may attract more birds

that may facilitate the regeneration of bird-dispersed rain forest plants (Luck and Daily

2003).

Connectivity of forest fragments through suitable habitat (e.g secondary forests)

may aid several sensitive species to survive in the short to middle term, allowing them to

move in between fragments (Stouffer et al. 2006), but there is no guarantee that all

species will survive in the long term (Stouffer et al. 2006; Sigel et al. 2006). For instance,

even a large reserve (La Selva in Costa Rica – 1611 ha), despite a forested connection to

Braulio Carrillo National Park (45,000 ha), is apparently too small to even maintain all

species of one major guild (understory insectivores) (Sigel et al. 2006). Therefore, since

the PTBC (80,000 ha) has less than 50,000 ha under forest cover and struggles with large

residential projects, large efforts are required to maintain and enhance connectivity in

order to achieve effective diversity conservation, especially for the species that are more

susceptible to fragmentation or those that need large habitat areas to survive in the long

term.

117
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Table 4.1 Bird abundance and species richness by habitat guilds in 10 land-use types in the Path of the Tapir Biological

Corridor, Costa Rica. Data are averages per census (N=12).

Forest Specialist Forest Generalist Open Area Species

Species Species Species


Land Use Richness Abundance Richness Abundance Richness Abundance
W Refuge 56.2 (0.8)a 231.3 (8.9)a 13.6 (1.7)e 34.9 (5.6)d 0.7 (0.3)f 2.1 (1.1)e
B Reserve 55.4 (1.4)ab 210.6 (9.4)a 12.6 (1.1)e 36.8 (4.4)d 1.1 (0.4)f 2.3 (0.9)e
F Edge 50.4 (1.4)b 204.5 (7.6)a 27.8 (1.9)cd 79.8 (9.8)c 3.9 (0.5)f 10.9 (1.8)bc
F Fallow 30.8 (1.2)c 112.5 (7.1)b 39.1 (2.3)ab 188.3 (10.3)ab 14.3 (0.7)d 79.4 (5.2)ab
T Plantation 24.3 (1.0)d 54.3 (5.6)c 27.2 (1.6)cd 103.8 (8.5)bc 10.3 (0.6)e 61.8 (6.3)b
Homegarden 21.3 (1.6)d 70.8 (4.7)bc 43.3 (1.8)a 234.4 (9.1)a 22.0 (0.7)b 264.3 (8.6)a
R Tourism 15.8 (1.2)e 52.7 (3.9)c 29.5 (1.4)bcd 139.1 (8.93)b 17.8 (0.6)c 153.7 (7.8)a
Silvopastoral 12.1 (1.2)e 32.9 (4.1)d 35.9 (2.2)b 188.9 (10.8)ab 26.7 (0.6)a 268.4 (6.4)a
Oil Palm 5.2 (0.7)f 9.8 (1.3)f 24.7 (1.1)d 111.6 (5.3)bc 21.3 (0.6)b 221.3 (7.9)a
Village 5.1 (0.8)f 17.5 (1.8)e 26.9 (1.1)cd 146.3 (10.9)b 22.1 (0.6)b 324.9 (9.1)a

Values represent accumulated average values for each of the 12 censuses conducted and they are followed by standard
errors in parentheses. Different letters mean statistical differences with an α < 0.05.

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Table 4.2 Bird abundance and species richness by feeding guild in 10 land-use types in the Path of the Tapir Biological

Corridor, Costa Rica. Data are averages per census (N=12).

Frugivores Insectivores Nectarivores Granivores Carnivores


Land
Use Species Abundance Species Abundance Species Abundance Species Abundance Species Abundance
ASP 20.7 (1.0)cd 152.3 (10.3)bc 34.3 (2.0)abc 182.0 (9.1)ab 4.8 (0.4)bc 9.8 (0.7)de 9.3 (0.4)a 116.9 (9.2)a 4.6 (0.3)a 13.9 (1.9)a
BR 22.5 (0.9)bc 95.5 (6.0)d 36.8 (1.4)ab 134.3 (7.5)bc 6.1 (.3)b 14.0 (1.0)cd 2.3 (0.3)c 3.7 (0.5)d 1.5 (0.4)c 1.8 (0.5)e
FE 26.1 (1.1)ab 120.8 (9.0)cd 40.5 (2.3)a 142.3 (8.2)bc 9.4 (0.7)a 20.5 (1.7)ab 3.2 (0.2)c 7.3 (0.9)c 2.7 (0.3)bc 3.8 (0.5)de
FF 25.8 (0.8)abc 157.9 (7.9)b 40.3 (2.4)a 144.1 (9.0)bc 8.8 (0.5)a 19.3 (1.6)bc 7.3 (0.4)b 53.4 (4.8)b 1.8 (0.2)c 5.2 (0.7)cd
HG 28.2 (0.9)ab 247.7 (6.2)a 35.9 (2.5)ab 191.7 (9.7)a 10.1 (0.6)a 25.5 (1.6)a 8.3 (0.4)ab 68.9 (6.0)ab 3.0 (0.2)bc 6.1 (0.7)bcd
OP 11.2 (0.4)e 63.3 (5.4)e 23.6 (1.2)cd 148.3 (6.9)ab 2.0 (0.4)c 3.2 (0.7)e 8.8 (0.4)ab 104.4 (7.2)a 3.8 (0.3)ab 10.2 (1.0)ab
RT 20.3 (0.9)c 146.8 (5.8)bc 26.6 (1.5)cd 123.6 (7.9)bc 5.8 (0.5)b 13.6 (2.1)cd 7.3 (0.3)b 51.5 (4.6)b 2.4 (0.3)bc 5.6 (0.8)bcd
TP 17.5 (0.9)d 84.2 (6.2)d 31.8 (1.9)bc 114.7 (10.3)c 5.8 (0.5)b 11.8 (1.0)d 3.6 (0.4)c 10.9 (1.2)c 2.7 (0.4)bc 8.3 (0.9)abc
VI 17.1 (0.6)d 184.8 (8.5)b 19.8 (1.1)d 147.1 (7.5)ab 3.4 (0.3)c 7.2 (0.7)e 8.1 (0.5)ab 55.8 (5.3)b 3.8 (0.4)ab 11.8 (2.0)ab
WR 20.8 (1.0)cd 98.5 (4.9)d 38.3 (1.7)ab 149.8 (9.2)ab 6.3 (0.4)b 12.4 (0.8)d 2.1 (0.1)c 4.0 (0.5)d 3.0 (0.5)bc 3.6 (0.6)de

Values represent accumulated average values for each of the 12 censuses conducted and they are followed by standard errors in parentheses. Different
letters mean statistical differences with an α < 0.05.

ASP = Agrosilvopastoral systems; BR = Biological Reserves; FE = Forest Edges; FF = Forest Fallows; HG = Homegardens; OP = Oil Palm; RT =
Residential Tourism Projects; TP = Tree Plantations; VI = Village; WR = Wildlife Refuges

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Figure 4.1. Relative abundance of species by habitat guild (percentage of species)

within 10 land-use types in the Path of the Tapir Biological Corridor, Costa Rica

125
sp29

1.0

sp19
0.5

TP OP
sp12
NMDS2

sp23
sp21
sp52 sp45
sp38
sp5 sp49 sp17
sp1
sp55
sp6 sp24
sp11
sp39
0.0

sp36 sp41
sp28 sp48
BR sp31
WR sp8 RT
FE HG sp27
sp2
sp40
sp20
sp22
sp14
sp30
sp53
sp25
sp35
sp13 FF ASP
sp34
sp15
sp26
sp46
sp54 sp9 sp16
sp50
sp4 sp51 sp44
sp10
sp42 sp47 sp33
sp43 sp3
sp32 sp56
sp7
sp18 VI
-0.5

sp37

-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5

NMDS1

Figure 4.2 Non-metric multidimensional scaling (NMDS) ordination of the

distribution of canopy forest specialist species in ten land-use types in the Path of

the Tapir Biological, Corridor.

BR = Biological Reserve; WR = Wildlife Refuge; FE = Forest Edge; FF = Forest Fallow; TP = Tree


Plantation; HG = Homegarden; ASP = Agrosilvopastoral System; RT = Residential Tourism; OP =
Oil Palm Plantation; VI = Villages. Numbers represent species (See Appendix 1)

126
1.0
sp34

sp78
0.5

OP
sp38
sp26
sp72
sp59 sp66
NMDS2

FF
sp57

sp16 sp49sp22 sp17


sp31
sp32
sp5
sp53
sp45 sp40 sp28
sp55
sp70
sp20 sp18 WR
sp60 sp64 sp9 sp69
sp56 sp25
sp21
sp63sp50 sp14
0.0

sp8
sp65sp3 sp7 sp15
sp76 sp43 sp46 VI
BR sp19
sp13sp36 sp29 HG sp12
sp71
sp10
sp67
sp54 sp30
sp73
sp77
sp74
sp75
sp6
sp61
sp62
sp44 sp35 sp33 sp42
FE sp2 RT sp4
sp51
sp27
sp37
sp23 TP
sp58
sp52
sp48
sp39 sp68
sp11
sp47 sp24 sp41

ASP
-0.5

sp1

-1.5 -1.0 -0.5 0.0 0.5 1.0

NMDS1

Figure 4.3 Non-metric multidimensional scaling (NMDS) odination of the

distribution of understory forest specialist species in ten land-use types in the Path

of the Tapir Biological, Corridor.

BR = Biological Reserve; WR = Wildlife Refuge; FE = Forest Edge; FF = Forest Fallow; TP = Tree


Plantation; HG = Homegarden; ASP = Agrosilvopastoral System; RT = Residential Tourism; OP =
Oil Palm Plantation; VI = Villages. Numbers represent species (See Appendix 1)

127
Figure 4.4 Relative abundance of bird species by feeding guild (percentage of

species) within 10 land-use types in the Path of the Tapir Biological Corridor, Costa

Rica

128
Figure 4.5 Relative abundance of birds (percentage of birds) for activity within 10

land-use types in the Path of the Tapir Biological Corridor, Costa Rica

129
Figure 4.6 Relative abundance of birds by microhabitat (percentage of birds) within

10 land-use types in the Path of the Tapir Biological Corridor, Costa Rica

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Chapter 5

Conservation of Threatened and Endemic Bird Species in a Human-Modified


Biological Corridor: Sustainable Forestry Criteria Recommendations

Abstract

Conservation of threatened and endemic species is a priority at the local, national,

and global levels, especially in the current human-modified landscapes. These groups of

species are relevant because they are intolerant of forest fragmentation and land-use

change and identification of their habitat preferences is important for their conservation.

This chapter will describe the status of endangered, threatened, and endemic bird species

found in the Path of the Tapir Biological Corridor, Costa Rica. In addition, based on

species habitat preferences and following sustainable forestry criteria, a series of

recommendations are described for conservation of bird species, and also for other

species of conservation concern. Using 200 sampling counts at ten different land-use

types (wildlife refuges, biological reserves, forest edges, forest fallows, tree plantations,

residential tourism projects, villages, oil palm plantations, homegardens, and

agrosilvopastoral systems), 32 threatened species and 22 endemic species were identified.

Eight of the 22 endemic species were also under threat, and three endangered species

were registered: Ara macao, Amazilia boucardi, and Icterus mesomelas. Overall, 64%

and 75% of endemic and threatened species, respectively, were forest-dependent species.

Moreover, frugivores and insectivores were the most abundant guilds across endemic and

threatened species. When the habitat dependency of bird species and the socio-political

and economic situation in the PTBC were considered, based on concepts of sustainable

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forestry, it was assessed that the corridor could be sustainable if the natural resources are

managed in three units that includes protected areas, integrated management areas, and

tree plantations. Using payment for environmental services, ecotourism, reforestation,

environmental education programs, and promoting national and foreign investment in the

region, among other strategies, could provide the rural infrastructure that local people

need to practice integrated management effectively.

Introduction

Fragmentation and isolation of Costa Rican protected areas are jeopardizing

biological conservation (Powell et al. 2000; Sanchez-Azofeifa et al. 2003). Therefore,

given these limitations of the protected area system, there is a pressing need to study

biodiversity and improve management not only within protected areas’ boundaries, but

also in the fragmented landscape matrices that surround them. However, because of the

complexity of human-modified landscapes, especially in the tropics, there are no generic

recipes that can be applied appropriately everywhere for conservation planning

(Lindenmayer and Franklin 2002; Lindenmayer 2009).

Threatened species (Gaston and Blackburn 1996), endemic species (Myers et al.

2000), and small geographic range species (Rendijo 2001) should be considered as

priorities for conservation planning. These groups of species are relevant because they

are intolerant of forest fragmentation and land-use change (Rendijo 2001) and

identification of their habitat preferences is important for their conservation (Gaston and

Blackburn 1996). Moreover, although it may take a century for all sensitive species to be

extirpated from a site following habitat loss, species with larger or heavier bodies and

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those foraging on insects, fruits, or both are particularly extinction prone, and therefore

should also be considered within sustainable forest management practices (Sodhi et al.

2004).

This chapter will describe the status of endangered, threatened, and endemic bird

species found in the PTBC. In addition to assessing the status of species of concern, some

alternatives for their conservation following sustainable forestry criteria developed by

Oliver (2003) and Oliver and Deal (2007) will be described. The goals of sustainable

forest management are to provide a steady flow of resources and income, while

preserving forest cover, biodiversity and ecosystem integrity (Oliver 2003). According to

Oliver and Deal (2007) two ways of discussing sustainable forestry have been proposed.

The first approach (Venn diagram approach) considers sustainable forestry as

overlapping acceptable ecological, economic, and social activities. The second approach,

known as the matrix approach, ensures that one ecosystem is neither hoarding nor overly

exploiting forest values to the detriment of itself or other ecosystems (Oliver and Deal

2007).

Based on the PTBC’s conservation objectives, recommendations are described for

conservation of endangered and endemic species while managing existing resources. The

recommendations may be applicable to other human-modified landscapes with similar

ecological, political, and socio-economic features. The criteria include biodiversity

analysis and the status of the threatened and endemic species found in the PTBC,

socioeconomic benefits, productive capacity, forest health, soil and water quality, and

carbon sequestration in the region (Oliver 2003).

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Methods

Study area: Path of the Tapir Biological Corridor

Conservation objectives

The corridor’s main objective is to create a network of sites favorable to fauna

and flora between the forests of the Osa Peninsula and Golfo Dulce, including Corcovado

National Park. These forests connect with those located in the Los Santos Forest Reserve

in the Talamanca Mountain Range. In addition, the PTBC was created as a means to

achieve four major goals (TNC-ASANA 2000; Redondo-Brenes 2007a): (1) Restore

natural habitats to enable the return of terrestrial endangered species and marine species

to the forests and beaches they inhabited half a century ago, and protect existing species

by allowing local populations to become more robust; (2) Halt deforestation within the

corridor and restore forests in order to complete the corridor and protect water sources for

use by communities, particularly in watersheds and groundwater recharge zones; (3)

Encourage local communities to value resources and use them sustainably; and (4)

Reduce and prevent soil erosion to benefit local farmers and for biodiversity conservation

in rivers, mangroves, and coral reefs within the region, especially in Marino Ballena

National Park.

Corridor justification

According to TNC-ASANA (2000), there are four main elements that justify the

creation of the PTBC: (a) providing connectivity between protected areas, (b) protecting

endemic species, (c) protecting endangered species, and (d) promoting sustainable

management of natural resources.

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Providing connectivity between protected areas

One of the main problems with the protected areas system in Costa Rica is the

isolation of most of these areas (Sanchez-Azofeifa et al. 2002a, 2003). The PTBC, which

is a part of the multinational Mesoamerican Biological Corridor, was proposed with the

intent of diminishing the negative effects of fragmentation and habitat loss in the Central

and South Pacific regions of the country by providing connectivity through several forest

remnants (e.g., privately-owned protected areas as stepping-stone corridors) to protect

areas such as Corcovado National Park, Piedras Blancas National Park, the Terraba-

Sierpe Wetlands, and Golfo Dulce and the Los Santos Forest Reserves.

Protecting endemic species

According to a rapid ecological assessment (TNC-ASANA 2000), the PTBC area

has a moderate level of endemism in comparison with other areas of the country such as

Corcovado National Park. For example, the PTBC provides habitat to 6 plant species

endemic to Costa Rica. From the 26 amphibian species found in the PTBC, four species

are endemic to the country and another four are found only in the area between Nicaragua

and Panama. In addition, one mammal, eight reptiles, and 11 bird species endemic either

to Costa Rica alone or jointly to Costa Rica and Panama are also found in the corridor

area. Finally, special attention needs to be placed on fish species since the corridor has 13

endemic species, representing 68.4% of the freshwater endemic species of the country.

135
Protecting threatened and endangered species

As a result of habitat loss, fragmentation, and illegal and legal hunting and

poaching, a total of 38 species of flora and fauna are considered either threatened or

endangered species in the region (IUCN 2009). Within the 38 species, there are six trees,

three amphibians, seven reptiles, 10 birds, and 12 mammals. According to the 2009

IUCN Red List of Threatened Species, the study area provides habitat to several

endangered bird and mammal species such as the squirrel monkey (Saimiri oerstedii),

yellow-billed cotinga (Carpodectes antoniae), and mangrove hummingbird (Amazilia

boucardi). In addition, the turquoise cotinga (Cotinga ridwayi) and the three-wattled

bellbird (Procnias tricarunculata) are considered vulnerable species, and the black guan

(Chamaepetes unicolor), the great curassow (Crax rubra), baird’s trogon (Trogon

bairdii), the harpy eagle (Harpia harpyja), and the jaguar (Panthera onca) are listed as

species near threatened (IUCN 2009). Other species of concern in the IUCN list found in

the region and considered priority species for conservation in Costa Rica are margay

(Leopardus wiedii), ocelot (Leopardus pardalis), scarlet macaw (Ara macao), and spider

monkey (Ateles geoffroyi).

Promoting sustainable management of natural resources

Aside from the ecological justifications such as biodiversity protection, there were

at least two socio-economic aspects relevant for the creation of PTBC: water-soil

protection and ecotourism. This area has more than 30 rivers, all of which provide

potable water for domestic consumption and water used in agriculture practices,

especially in the corridor lowlands. Thus, it is justifiable to protect the corridor highlands

136
in order to secure water quality for its inhabitants, especially because to date local people

see water scarcity and quality as an issue in the region (Welsh 2006). Secondly,

ecotourism is growing in the region and this is very important because it provides new

job opportunities for local people. Even when not considering rivers, this area still has

more than 50% of the landscape under forest cover. It also provides the visitors with

waterfalls and more than 70 km of coastline.

Land-use types part of this study

For this chapter, I used the same ten habitat types and their corresponding 20

point counts per land-use type described in Chapter (3): forest edges, forest fallows,

wildlife refuges, biological refuges, tree plantations, villages, oil palm plantations,

residential tourism projects, agrosilvopastoral systems, and homegardens.

Identification of bird species of concern

Species of conservation concern

The list of species of concern described above is based on the IUCN Red List.

However, at the regional level, this list gets larger when the list of species that are

considered under any threat at the country level is included, especially for bird species.

For instance, Obando (2008) recently cited that 9.6% and 1.8% of total bird species in

Costa Rica are threatened and endangered species in the country, respectively. The

Ministry of Environment 2005-Decree lists 81 bird species under the category of

vulnerable or threatened species, and 17 bird species under endangered status. From this

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list of species under category of conservation concern, a total of 32 were identified in the

Path of Tapir Biological Corridor (Table 5.1).

Endemic species

In terms of endemism, Costa Rica is considered a restrained country (Obando

2008). Only 1.3% of all species are endemic to the country, birds being the group that

encompasses the lowest proportion (0.7%). However, about 10% of the bird species that

inhabit Costa Rica have very limited ranges and are considered regionally endemic –

most are only found in the southern part of Central America and nowhere else in the

world (Garrigues and Dean 2007). In the PTBC only one species endemic to the country

was identified (mangrove hummingbird – Amazilia boucardi), but 21 regionally endemic

species were registered for this study (Table 5.2).

Data analysis

When analyzing bird relative abundance, the one way ANOVA test was used to

determine if there were statistical differences across the 32 species of conservation

concern and across the 21 endemic species. Abundance was estimated at the census level,

which means the cumulative number of birds per species per the 20 points within each

land-use type was used. Non-metric multidimensional scaling (NMDS) analyses were

conducted to assess the bird species preferences within the ten land-use types.

In addition, a series of graphs were created in order to compare the relative

abundance of total threatened and endemic species by feeding and habitat guilds. Bird

species were classified in three habitat guilds: forest specialist species, forest generalist

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species, and open area species. Forest specialist species mostly utilize closed-canopy

forests. Forest generalist species can occupy closed-canopy forests as well as forest edges

and clearings. Open-area species are not found in forests, but frequent areas where trees

are present. Classification of bird habitat preference was based on Stiles and Skutch

(1989) and Garrigues and Dean (2007). On the other hand, bird species were classified

based on their primary diet preference as frugivores (e.g. fleshy fruits), nectarivores

(nectar), carnivores (large arthropods and vertebrate prey), granivores (seeds and nuts),

and insectivores (small arthropods), following Stiles and Skutch (1989) and Garrigues

and Dean (2007).

All statistical analyses were conducted in PAST v 1.95 (Hammer et al. 2001) and

the NMDS were performed in R statistical software.

Results

Species of conservation concern

Overall, of the 334 bird species found in the PTBC (Chapter 3), 32 species (9.6%)

were classified in at least two categories of conservation concern (threatened or

endangered species, Table 5.1), and 22 species (6.6%) were classified as regionally

endemic (Table 5.2). Only eight endemic species were also considered under threat:

baird’s trogon (Trogon bairdii), crimson-fronted parakeet (Aratinga finshi), golden-naped

woodpecker (Melanerpes chrysauchen), mangrove hummingbird (Amazilia boucardi),

three-wattled bellbird (Procnias trinarunculatus), white-throated shrike-tanager (Lanio

leucothorax), yellow-billed cotinga (Carpodectes antoniae), and turquoise cotinga

(Cotinga ridwayi).

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Of the 32 species of conservation concern, only three were considered endangered

species at the national level: mangrove hummingbird, scarlet macaw (Ara macao), and

yellow-tailed oriole (Icterus mesomelas). Bird abundance across species was statistically

different (p < 0.05; Figure 5.1). For the species of conservation concern, orange-chinned

parakeet (Brotegeris jugularis) was the species with the highest abundance, followed by

white-crowned parrot (Pionus senilis), red-lored parrot (Amazona autumnalis), crimson-

fronted parakeet (Aratinga finschi), mealy parrot (Amazona farinosa) (all Psittacidae),

and golden-naped woodpecker (Melanerpes chrysauchen). The other 26 species did not

have statistically significant abundance differences and 16 of these species had less than

1 bird registered per census. This means less than 1 individual was observed in 33.3

hours (200 points).

As for endangered species, one endemic species had a statistically large difference

in abundance with respect to the other species in this category (Figure 5.2). Cherries

tanager (Ramphocelus costarricensis) was not only the most abundant endemic species,

but also the most common species for the region (Chapter 3). Moreover, there was a

group of 16 species with no statistical differences in their abundance, and nine of these

had less than 1 individual observed per census. Other endemic species with intermediate

population sizes were yellow-crowned euphonia (Euphonia luteicapilla), black-hooded

antshrike (Thamnophilus bridgesi), and riverside wren (Thryothotus semibadius).

When species compositions were compared by guilds, relative species abundance

in different guilds was more consistent by habitat guilds than by feeding guilds (Figure

5.3; 5.4). For instance, the majority of endemic (64%) and threatened species (75%) were

forest specialists, and consequently, the minority was classified as forest generalist or

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open area species. In contrast, when feeding guilds were compared, endemic species had

similar relative species abundances across categories, but the threatened species were

primarily frugivores (53%), followed by insectivores (25%), and then carnivores (15.6%).

However, as anticipated, frugivores and insectivores together made up the majority for

both endemic and threatened species. Furthermore, no carnivore or granivore species was

endemic to this region; and although there were six endemic nectarivorous species, only

the mangrove hummingbird was also considered an endangered species. Of the other

seven endemic species classified as threatened species, only the crimson-fronted parakeet

(frugivore) was an open area specialist, while the other six species were forest-dependent

species. Four of them were also frugivores (yellow-billed cotinga, turquoise cotinga,

bellbird, and baird’s trogon) and two (golden-naped woodpecker and white-throated

shrike-tanager) were insectivores.

Despite the theoretical habitat classification for endemic species and species of

conservation concern described above, several species utilized more than one habitat

(beyond expected) across the ten habitat types assessed. While in forested habitats, 24

species of conservation and 19 endemic species were observed, in human-modified

landscapes 20 species of conservation concern and 18 endemic species were registered.

Similarly, utilization of the different land-use types varied across bird species. For

instance, even though there were 28 forest species (specialist and generalist together) of

conservation concern, three of these species (turquoise cotinga, yellow-billed cotinga,

and scarlet macaw) were not recorded in forested habitats, but were found in human-

modified landscapes. In fact, 20 forest species from this group utilized at least one

human-modified land-use type, and the multivariate ordination depicted that at least 10

141
out of 32 threatened species were associated with six of the human-modified land-use

types (Figure 5.5).

Land utilization of endemic species was similar to the pattern of threatened

species. Several forest-dependent and generalist species were using human-modified

habitats. At least nine out of 22 endemic species could be associated more with human-

modified habitats than forested habitats (Figure 5.6).

Discussion

Use of Sustainable Forestry Concepts in the PTBC

Many frameworks and approaches are found in the literature concerning the best

landscape management practices (i.e. sustainable forestry) to simultaneously maintain

forest biodiversity, ecological functions, and human livelihoods (Hunter and Calhoun

1996; Campos et al. 2001; Noss 2001; Putz et al. 2001; Lindenmayer and Franklin 2002;

Oliver 2001, 2003; Dudley et al. 2005; Higman et al. 2005; Hagan and Whitman 2006).

Regardless of the authors’ background, affiliation, standpoint, or perspective, a common

goal within sustainable forest management is to protect biodiversity. According to

Higman et al. (2005), sustainable forestry can be defined as the forest management

practices that provide goods and services from a forest ecosystem without degradation of

site quality, and without a decline in the yield of goods and services over time. Similarly,

Oliver (2003) mentioned that the definition of sustainable forestry has its roots in the

concept of environmental justice. In other words, people living in one place and time

should provide their “fair share” of values –neither unfairly exploiting nor depriving

themselves of certain values to the detriment or benefit of people in another place or time.

142
Achieving a sustainable forestry goal will probably take time as people agree on what

sustainability means at the global, sub continental, national, and regional scales (Oliver

2001).

Aside from timber and biodiversity, forested lands provide other environmental

goods and services such as carbon sequestration, soil and water protection, scenic beauty,

food provision (Groot et al. 2002), and jobs for rural people (Oliver 2003), among others.

However, most of these goods and services as well as biodiversity are being threatened

by habitat loss and the fragmentation of natural habitat by humans (Groom et al. 2005),

along with climate change, nitrogen deposition, and invasive species (Sala et al. 2000).

And as a result of these threats, the conservation community is working with other

stakeholders including government agencies, industry groups, forestry schools, and

consumers of forest products to develop conservation-planning strategies for biodiversity

conservation (Gordon et al. 2005). The main goal is to protect habitats, to maintain

biological diversity, to preserve ecological functions, and to ensure sustainable forest

management in managed areas (Oliver 2003; Gordon et al. 2005). Unfortunately, even

though many of these concepts have been implemented in temperate regions, little is

known about how tropical forests can be best managed to enhance biodiversity (Putz et

al. 2001). But, some recent forest sustainable management projects implemented in the

tropics have sent a positive message about its feasibility (Frost et al. 2006, Dennis et al.

2006, Peña-Claros et al. 2008; Fonseca et al. 2009).

This discussion focuses on the status and habitat requirements of the threatened

and endemic species in the PTBC, by providing an analysis of socio-political and

economic factors that may affect the implementation of sustainable forestry following

143
Oliver (2003). The six criteria for achieving sustainable forestry described by Oliver

(2003) are evaluated: biodiversity (protecting habitats for endangered/endemic species),

socioeconomic benefits, productive capacity (wood and non-wood), forest health, soil

and water quality, and carbon sequestration.

Biodiversity conservation of endangered and endemic species

Biodiversity conservation has become the stated objective of national

governments, state agencies, local communities, and scientific organizations (Redford

and Richter 1999). According to Dirzo and Raven (2003), the global state of biodiversity

is important because biodiversity is a central component of Earth’s life support systems

and directly relevant to human societies. Any attempt to defend a social cause, such as

biodiversity, should rest on the best facts available; and the loss of biodiversity is the only

truly irreversible global environmental change the Earth faces today. Moreover, Powell et

al. (2002) mention that biodiversity has intrinsic values and provides practical benefits

such as (1) medicines, plant derivatives and other timber and non-timber products, (2) a

basis for medicinal bioprospecting, (3) pollination and resilience to agricultural systems,

and (4) soil building and nutrient cycling processes. Moreover, since biodiversity has

social value, from recreation to spiritual and cultural benefits, it is increasingly

recognized as fundamental to human health (Powell et al. 2002), and this is a reason to

protect forested lands.

In order to evaluate the role of human-modified land-use types for biodiversity

conservation, it is important to know not only how many species are present within these

systems, but also which species are present and whether any of these species are of

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conservation concern (Petit et al. 1999; Harvey and Gonzalez Villalobos 2008). For the

PTBC, a total of 46 out of 334 species were classified as either threatened/endangered or

regionally endemic species, including eight species that are endemic and under threat.

Among the 46 species, they differed in diet and habitat preference as well as their

conservation priority within the corridor’s conservation goals. For instance, conservation

efforts may not focus on species like the cherries tanager, which despite being an

endemic, forest generalist, and frugivorous species, was the most abundant species in this

study (Chapter 3), and was found in eight land-use types, excluding the interior of

wildlife refuges and biological reserves. However, their role as seed dispersers of small

seeds may be relevant to catalyze secondary succession in the region.

In addition, the eleven species of the Psittacidae family registered in this study are

categorized as being of conservation concern or endangered (e.g. Ara macao) as a result

of habitat loss, direct hunting, and poaching for the pet trade market (Stiles and Skutch

1989; Garrigues and Dean 2007). However, most of these species were observed in more

than one habitat type and the majority of them had high populations when compared not

only to endemic and endangered species, but also across all species in the corridor

(Chapter 3). For most of these species, decreased hunting pressure was mentioned by

local people as one of the main reasons for such high populations compared to the last

10-20 years. Within this family, of greater concern are Pionopsitta haematotis, mostly

found in private reserves, and Ara macao, which once resided on both the Pacific and

Caribbean slopes, and now is only located in a few spots along the Pacific Coast (Stiles

and Skutch 1989; Vaughan et al. 2006; Garrigues and Dean 2007). In addition, there have

been a few reports of this species in the Caribbean lowlands recently (Henderson 2010;

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Guindon, personal communication, April 2010). In the corridor, Ara macao populations

were located foraging and perching mostly in homegardens, villages, and in forest edges

in the southern part of the region. A few individuals were also registered in homegardens

of the PTBC’s northern limit; however, because the forests around these villages were not

surveyed, this species was not included as resident of forested habitats. Nevertheless, as

part of this study, macaws were observed in a few forest patches north of where they

were recorded.

Reintroduction of this species is being assessed in the Hacienda Baru Wildlife

Refuge as part of a national reintroduction program run by Amigos de las Aves.

Hacienda Baru, along with forested areas around this refuge, provide the required food

sources as well as large trees (e.g. Ceiba pentandra) for nesting by scarlet macaws

(Castles et al. 2008). This program will increase the likelihood of connecting macaw

populations along the whole Central and South Pacific Coast of the country, thereby

increasing the probability of gene exchanges, and therefore contributing to the

survivorship of this species in the long term.

The other two endangered species Icterus mesomelas and Amazilia boucardi were

registered only once and twice, respectively, over the duration of this project. Icterus

mesomelas is a forest-generalist, insectivore species that forages in thickets and second

growth near water, but is considered a rare resident of the Caribbean lowlands of Costa

Rica (Garrigues and Dean 2007). However, this is not the only record of this species in

the PTBC, it has been reported as part of the Annual Christmas Count, suggesting that

this species as well as several others (e.g. hoffmann’s woodpecker (Melanerpes

hoffmanii), rusty-margined flycatcher (Myiozetetes cayanensis), blue-headed parrot

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(Pionus menstruus), white-throated magpie-jay (Calocitta formosa)) may be spreading in

the Central and South Pacific lowlands from the Caribbean and other regions of the

country (Ureña, 2005; Garrigues and Dean 2007).

On the other hand, A. boucardi is an endemic species of the Pacific coast of Costa

Rica, specifically mangroves and adjacent forests (Garrigues and Dean 2007).

Unfortunately for this species and many others that are mangrove-dependent

(Nagelkerken et al. 2008), these habitats are illegally disappearing for agricultural

expansion and residential development, despite mangrove forests being considered

protected areas in Costa Rica (Redondo-Brenes and Villalobos 2008). Throughout the

two years I spent in the PTBC, I participated in at least four inspections where damages

to mangroves were found, including drainage, canalization, land-use change, etc. Where

mangroves are native, similar patterns are happening everywhere in the tropics,

jeopardizing the ecological functions these ecosystems provide to people and the

environment (Nagelkerken et al. 2008).

Other bird species whose conservation is also at risk include those that occur only

in large patches of forests and that are absent from small patches with little or no true

interior habitat, as well as non-flying species with poor dispersal abilities (Laurance

2004). Some of these species found in the PTBC were Procnias tricarunculatus,

Spizaetus ornatus, Buteogallus urubitinga, Sarcoramphus papa, Cotinga ridgwayi,

Carpodectes antoniae, Penelope purpurascens, Crax rubra, Micastur semitorquatus,

Deconychura longicauda, Laniocera rufescens, Odontophorus gujanensis, Pionopsitta

haematotis, Lophostrix cristata, Tinamus major, and Trogon bairdii. From this group of

species, more attention should be placed on P. purpurascens, C. rubra, Procnias

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tricarunculatus, and T. bairdii because of their role as large-seed dispersers (Chapter 4;

Guindon 1997; Jimenez et al. 2003; Primack and Corlett 2005). Furthermore, forested

habitats are not only relevant because they provide habitat for these endangered/endemic

species listed above, but also for several understory species that do not cross the matrix,

including army ant followers and members of mixed-species flocks that strongly avoid

forest edges (Rendijo 2001; Laurance 2004). Some of these species, with small

populations in this study, were bare-crowned antbird (Gymnocichla nudiceps), bicolored

antbird (Gymnopithys leucaspis), black-faced antthrush (Formicarius analis), buff-

throated foliage-gleaner (Automolus ochrolaemus), russet antshrike (Thamnistes

anabatinus), streak-chested antpitta (Hylopezus perspicillatus), among many other

species.

Unfortunately, urban and tourism development are jeopardizing the conservation

of many of these species in the region, especially because forest cover is either

disappearing or being fragmented around most private reserves (Redondo-Brenes 2007a;

Redondo-Brenes and Villalobos 2008). Therefore, implementation of sustainable forest

management may provide not only a larger chance for these species to survive, but also

more incentives to local stakeholders to protect natural habitats.

Socioeconomic Benefits

According to Oliver (2003), socioeconomic benefits and biodiversity are two

main criteria used in sustainable forestry approaches such as the Montreal Process

Criteria. The main goal is to integrate socioeconomic benefits and biodiversity from a

local and a global perspective, especially because many scales need to be considered to

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ensure that actions at one place or scale create positive consequences elsewhere (Oliver

2003). In other words, the goal here is to protect forested reserves for biodiversity while

obtaining economic benefits from these reserves as well as other managed landscapes

such as agricultural fields and tree plantations. Accomplishing these sustainable forestry

practices in a tropical region will need to consider several points within the agenda.

First, the potential conflicts between conservation and human welfare that have

alienated potential allies in the past have to be avoided, especially in human-dominated

landscapes in tropical regions (Brandon and O’Herron 2004; Anderson and Jenkins 2006;

Hilty et al. 2006; Chang et al. 2007). Second, it has to be stated that management for

some goods and services necessarily involves management against some others (Putz et

al. 2001). Therefore, several scenarios can be endeavored in the PTBC to achieve the

biodiversity and socioeconomic benefits criteria.

In a human-dominated landscape like PTBC, protected areas are interspersed

amongst other land-use scenarios such as residential development, pasture lands, tree

plantations, annual and perennial crops, and tourism projects, among others. One of the

first steps is to analyze how to create or to ensure a network connects the more than 30

privately-owned protected areas and Marino Ballena National Park within the PTBC

(Reserves concept in Oliver 2003), and also to provide buffer zones for adjustment of

reserves boundaries (Noss 2001). The reserves can be connected using either natural

regeneration of abandoned agricultural lands or reforestation of those degraded lands

with native species through payments of environmental services (PES). At present,

FONAFIFO, the Costa Rican government institution in charge of the PES program, is

paying a total of US$64/ha/year towards natural forest protection, US$41/ha/year towards

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natural regeneration of abandoned lands, US$816/ha/5-year period towards the

establishment of tree plantations, and US$1.30/tree towards agroforestry systems

(FONAFIFO 2009). In the PTBC, the PES implementation has secured protection of

more than 5,000 ha from 1997 to 2008. From 1997 to 2002, payments to participants in

the region totaled nearly US$175,000 per year (Newcomer 2007). Although PES

programs are not designated for poverty reduction (Pagiola et al. 2005), for small local

farmers in the corridor, the earnings from the PES represent an important extra income,

especially when they have had a poor agricultural season because of the market prices or

weather conditions.

Despite the fact that PES has been a good source of income for several program

participants, and has helped to protect forests in the corridor, the PES scheme currently

used in Costa Rica needs some re-structuring. Poor funding (e.g., the demand for PES is

much higher than the funding currently available), delays in payments, medium-term

time frames (e.g., PES contracts range from 5 to 10 years), disproportionate

representation of program participants by large farmers and forest owners, and some

mismatch between conservation areas defined by FONAFIFO and conservation priorities

within each region, are some of the flaws of the program (Zbinden and Lee 2005;

Newcomer 2007; Redondo-Brenes 2007a). Thus, either the government should create a

better framework for the PES, or the PTBC organizations should look for alternative

funding sources to provide economic incentives to owners willing to preserve their land

(Anderson and Jenkins 2006; Redondo-Brenes 2007a). When a PES program design is

well thought out and local conditions are favorable, there can be important synergies

between economic, social, and ecological benefits (Pagiola et al. 2006).

150
One of the main approaches to promote sustainable forestry in the region through

economic development (i.e. PES) could be to reduce the need for subsistence farming and

grazing (Oliver 2001) that ultimately would promote better land-use practices. Aside

from PES, alternatives seen as important to promote both human welfare and

conservation in the region include ecotourism, establishment of tree plantations and

agroforestry systems, and low impact logging.

Because of all the natural resources found in the PTBC, ecotourism has grown

very quickly in the region. Most of the privately-owned protected areas integrate

protection and ecotourism, generating an extra income for the protected areas owners and

the people depending on tourism. Many local people who previously depended on

agriculture now are working directly or indirectly in ecotourism. Overall, it is suggested

that ecotourism may potentially make a positive contribution to resource conservation at

the local, national (Weinberg 2002; Rivera 2004; Kruger 2005), and global scales (Hunter

and Shaw 2007). However, unsustainable urbanization can negatively affect the region if

it surpasses the carrying capacity of the land (TNC-ASANA 2000; Newcomer 2007;

Basso and Newcomer 2009). Therefore, proper land-use planning is necessary for the

region.

Reforestation programs can also provide economic benefits and contribute to

biodiversity conservation (Tiarks et al. 1998; Hartley 2002; Lamb et al. 2005; Carnus et

al. 2006), and in fact, within the Costa Rican Plan of Sustainable Forestry, reforestation

and agroforestry systems are a priority (Calvo 2009). Within the PTBC there are more

than 20,000 ha under pastures that could be used for reforestation programs. Although

most of the reforestation programs in Costa Rica have used exotic species, there are

151
several good examples of successful reforestation trials (Redondo-Brenes and

Montagnini 2006) and reforestation programs in small- and medium-sized farms with

native tree species (Redondo-Brenes 2007b; Streed et al. 2006). For example, Streed et

al. (2006), using native species within the PTBC, show that small-scale reforestation

(18.6 ha) with mixtures of native species can be financially profitable for both an investor

and a farmer/landowner, and increases biodiversity in the region through reduced-impact

management (Leopold and Salazar 2008).

Niewenhuyse et al. (2000) demonstrated the profitability of tree plantations in the

Caribbean lowlands of Costa Rica, as they found that melina (Gmelina arborea) and teak

(Tectona grandis) plantations were more profitable than pasture for beef production.

Aside from the economic benefits tree plantations can provide to landowners and the

increase in timber supply in Costa Rica, we also have to consider that tree plantations, if

not intensively managed, can provide habitat for wildlife (Carnus et al. 2006).

Furthermore, all tree plantations, including those of exotic species and those intensively

managed, are better for biodiversity conservation than degraded pasture lands (Gascon et

al. 1999; Ricketts et al. 2001; Lindenmayer and Franklin 2002; Lamb et al. 2005; Carnus

et al. 2006).

The last alternative for integrating biodiversity conservation and economic

benefits in the corridor is reduced-impact management of primary and old secondary

forests. At the landscape level, disturbance in some areas (i.e., forest logging) is

important for biodiversity management because it can provide habitat for some species,

especially wildlife species, that only inhabit open areas (Oliver et al. 1998). In addition,

Dunn (2004) proved empirically that reduced-impact logging appears to have much less

152
impact on faunal biodiversity (i.e., ants, birds, and lepidoptera) than conventional logging

or forest conversion to agriculture does. In Costa Rica, Campos-Arce et al. (2001) and

Campos-Arce (2006) mention that certified reduced-impact managed stands have

minimal effect on the habitat function that natural forests provide. This is based on

harvesting 4-6 trees/ha in a 15-year cycle, according to a 10-year study from researchers

of the Tropical Agricultural Research and Higher Education Center (CATIE) (Campos-

Arce et al. 2001; Campos-Arce 2006). Therefore, it would be possible to identify some

areas of primary forest and old-secondary forests in which local people can practice

reduced-impact logging, following the recommendations by Campos-Arce et al. (2001) to

mitigate the direct and indirect effects of harvesting on biodiversity. However, these areas

have to be outside protected areas and those connecting protected areas to ameliorate

negative effects (Noss 2001; Sekercioglu 2002).

Productive capacity

Even though Oliver (2003) states, (1) the world is consuming much less wood

than it is growing, (2) there seems to be a surplus of low quality temperate and tropical

hardwoods, (3) wood consumption is helpful by substituting for more fossil fuels-

consuming construction products made of steel, concrete, aluminum, and brick, (4) and

sustainable forestry can provide environmental friendly products and employment in rural

areas, the situation in Costa Rica is totally different as much more wood is consumed

than is growing in productive forests and tree plantations (Arce-Benavides and Barrantes-

Rodriguez 2004; Calvo 2009). In fact, the most recent State of the Nation report 2009

mentioned that after 2010 the timber deficit in the country will reach 850,000 m3/year as

153
a result of shortages of timber coming from tree plantations (main source of timber in the

country), agroforestry systems, and sustainable forest management (Calvo 2009). For this

reason, the forestry sector proposal includes a reforestation program of 7,500 ha/year and

the management of 150,000 ha of forests, using PES and also private investments (Calvo

2009). The current market requires both softwood and hardwood (Arce-Benavides and

Barrantes-Rodriguez 2004; Calvo 2009).

In the PTBC, low quality wood can be obtained from tree plantations established

with fast-growing timber species such as melina, or the native species Vochysia

guatemalensis and Vochysia ferruginea (Leopold et al. 2001; Redondo-Brenes and

Montagnini 2006; Redondo-Brenes 2007b). In addition, secondary forests can also be a

good source of this type of timber (Redondo-Brenes et al. 2001; Valenciano and

Redondo-Brenes 2006). On the other hand, high-quality wood can be obtained from

primary forests and tree plantations of species such as teak and Terminalia amazonia

(Healey and Gara 2003; Kanninen et al. 2004; Carpenter et al. 2004; Streed et al. 2006;

Redondo-Brenes 2007b). Unemployment in the region was roughly 6% in 2004

(Newcomer 2007), so management of both tree plantations and natural forests would

provide not only timber to the forestry industry, but also jobs for local people.

Forest Health

Sustainable forestry can be promoted by keeping fires, insect and disease

outbreaks, and exotic weed invasions to non-catastrophic levels by appropriate

management (Oliver 2003). In Costa Rica, even though there have been more than 1,500

plant species introduced in the country (Obando 2002), there have been no reports of

154
serious insect and disease outbreaks or exotic weed invasions in the PTBC. However,

human-caused forest fires are becoming very common in the dry months, affecting more

than 200 ha in 2009.

Soil and Water quality

Sustainable forestry can increase economic development by alleviating soil

erosion, compaction, and nutrient depletion associated with subsistence farming and

grazing (Oliver 2003). Erosion problems are easily detected in the PTBC landscape. The

main causes of erosion are overgrazing and erosion from clear-cut areas to build new

residential areas. Sediments from both sources are polluting water sources (e.g., rivers

and springs), jeopardizing not only water quality for people and cattle consumption, but

also killing fish and other aquatic organisms in rivers. Without appropriate plans for its

sustainable management and usage, water is at risk of increased scarcity and decreased

quality (Welsh 2006). Costa Rica has recently been facing many watershed issues

because of a rising population and increased demand for clean drinking water, combined

with unsustainable land-use practices (Sanchez-Azofeifa et al., 2002b). In the PTBC,

Welsh (2006), studying water sustainability in two watersheds, discovered that the

decrease in water quality in two major rivers was related to a lack of forest cover in the

region, and that soil sediments coming from degraded pasture lands were the main source

of pollution.

The introduction of trees either in tree plantation or agroforestry systems has been

a common practice in Costa Rica to improve soil properties (Redondo-Brenes 2005). In

the country, several studies on the effects of trees on soil properties have been conducted

155
in the last two decades (Stanley and Montagnini, 1999; Montagnini, 2000). Restoration of

the degraded lands in the corridor through natural regeneration or the establishment of

tree plantations or agroforestry systems will not only ameliorate the negative effects of

erosion on water sources, but it would also provide all the economic and ecological

benefits described in the previous sections. To date, restoration of degraded lands around

main drinkable water sources in the PTBC is being achieved with the participation of

local people (Redondo-Brenes 2007a). Soil degradation and water quality are priorities

in the region, and both are also used as a means of preserving and increasing forest cover

because local people have become more conscious about the negative effects of forest

cover loss and degradation (Newcomer 2007; Basso and Newcomer 2009).

Carbon sequestration

Growing trees and storing the timber both within the forest and in forest products

reduce carbon dioxide (Winjum and Schroeder 1997; Oliver 2003). In Costa Rica, studies

of carbon sequestration estimates have been done in secondary forests (Vilchez et al.

2008), pure and mixed native tree plantations (Redondo-Brenes and Montagnini 2006;

Redondo-Brenes 2007b), and agroforestry systems (Montagnini et al. 2005). Overall,

carbon sequestration rates in agroforestry systems, native tree plantation, and secondary

forests range from 1.5 to 7 Mg C/ha/year (Montagnini and Nair 2004; Redondo-Brenes

and Montagnini 2006; Redondo-Brenes 2007b; Vilchez et al. 2007). Redondo-Brenes and

Montagnini (2006) and Redondo-Brenes (2007b) found that because of species growth

patterns in tree plantations, carbon sequestration estimations reflect two scenarios. First,

if the objective is to accumulate carbon in the short term, species such as V.

156
guatemalensis and V. ferruginea are two of the best options because of their fast growth.

On the other hand, if the objective is to create long term carbon sinks, species such as D.

panamensis and C. brasiliense are the best option. Higher density stands are also a good

alternative when carbon sequestration is the main objective (Redondo-Brenes 2007b).

Managing native tree plantations for timber or carbon sequestration may create

conflict among local farmers, government agencies, and potential carbon offsets buyers,

especially under the PES programs (Pfaff et al. 2000; Redondo-Brenes 2007b). Lamb et

al. (2005) mention that planting to generate ecological services (e.g., carbon

sequestration) as well as goods (e.g., timber) is difficult because trade-offs must be made

between the productivity of the desired goods and the provision of ecological services,

and the techniques to achieve these simultaneous goals are still being developed. For

instance, while local farmers are receiving government incentives (e.g., PES) for

establishing tree plantations in Costa Rica, most local farmers perceive plantations as a

timber production tool, and only a few landowners consider their environmental services

to be a unique goal (Delgado 2002; Piotto et al. 2003). Thus, if the government agencies

are evaluating the possibility of selling carbon offsets to a third party, they have to clarify

the objectives of the reforestation programs and the proper manner to manage the

plantations (Redondo-Brenes 2007b). However, even tree plantations designed for timber

production temporarily store carbon, until it is released into the atmosphere after the

burning of the wood (Oliver 2001; Aune et al. 2005).

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Conclusions: Achieving Sustainability

The corridor could be sustainable if the natural resources are managed in a

gradation including protected areas, integrated management areas, and tree plantations

(Oliver 2003), also known as the Triad Approach (Seymour and Hunter 1999). These

three management units could provide the habitat required by the different wildlife

species in the corridor as well as create economic opportunities or incentives to protect

the PTBC habitats. Protected areas would be the core conservation areas for more

sensitive forest species. Integrated management areas such as agroforestry systems and

other agricultural areas would provide not only income for local people, but also habitat

for open-area species, and connectivity and buffer zones for forest fragments. Finally,

tree plantations would be used to restore degraded landscapes, to provide habitat for

wildlife species, buffer zones and connectivity to forested areas, and to provide goods

and services to local residents.

Using payment for environmental services, ecotourism, reforestation,

environmental education programs, and promoting national and foreign investment,

among others, in the region could provide the rural infrastructure that local people need

to practice integrated management effectively (Oliver 2003). However, it has to be

controlled such that ecotourism projects, agricultural practices, forest management, and

the new residential development projects do not exacerbate the natural resources through

fragmentation and/or degradation/destruction/pollution of forested ecosystems.

It is expected that after the world economic crisis ends forest cover will be

negatively affected in Costa Rica, especially in areas where tourism and agriculture are

the main source of income for local people (Calvo, 2009). In the case of the Path of the

158
Tapir Biological Corridor, this scenario is likely because tourism development has

delayed its expansion due to the crisis. However, because of lack of control from Costa

Rican authorities (Redondo-Brenes 2007a; Redondo-Brenes and Villalobos 2008) as well

as real estate and development sectors being focused on business rather than

sustainability (Basso and Newcomer, 2009), the future of forest cover and therefore

wildlife in the corridor is uncertain. Under the best scenerio, even if forest cover does not

reduce drastically, road and development would fragment the already fragmented

landscape further, affecting the species that require large areas of land connected to

forests to survive. Therefore, there is a need to adopt sustainable forestry practices to

reduce the impacts that development will cause at the landscape level. In addition, there

is a need to provide alternative management opportunities that ensure income for local

people as well as conservation of biodiversity, especially of the more sensitive species.

Conservation of forest cover in reserves and the establishment of tree plantations

and agroforestry systems, especially with native species, will provide many benefits to

society in general. Tropical trees integrating into the landscape as forest reserves, tree

plantations or as part of agroforestry systems (e.g., home gardens, living fences,

agrosilvopastoral systems, improved fallows) can serve diverse economic, social, and

ecological functions that may ultimately help reduce atmospheric CO2 accumulation,

restore degraded soils, protect water sources, protect and enhance biodiversity, contribute

to the wood supply, and improve human welfare (Oliver 2003; Lamb et al. 2005;

Redondo-Brenes and Montagnini 2006; Carnus et al. 2006; Redondo-Brenes 2007b).

159
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Table 5.1 Threatened and Endangered bird species found in the Path of the Tapir Biological Corridor
Common name Scientific name Family Guild Land-use in the PTBC
1 Baird's Trogon Trogon bairdii Trogonidae FR, FS BR, FE, FF, HG, WR, TP
2 Bat Falcon Falco rufigularis Falconidae CA, OA HG, ASP
3 Blue-headed Parrot Pionus menstruus Psittacidae FR, FG HG, VI
4 Brown-hooded Parrot Pionopsitta haematotis Psittacidae FR, FS BR, FE, ASP, WR
5 Collared Forest-Falcon Micrastur semitorquatus Falconidae CA, FS BR, FE, WR
6 Crested Guan Penelope purpurascens Cracidae FR, FS BR, WR
7 Crested Owl Lophostrix cristata Strigidae IS, FS FE
8 Crimson-fronted Parakeet Aratinga finschi Psittacidae FR, OA All
9 Golden-naped Woodpecker Melanerpes chrysauchen Picidae IS, FS All, except VI
10 Great Black-Hawk Buteogallus urubitinga Accipitridae CA, FS BR, WR
11 Great Curassow Crax rubra Cracidae FR, FS BR, FE, WR
12 Great Tinamou Tinamus major Tinamidae FR, FS BR, FE, FF, OP, WR, TP
13 King Vulture Sarcoramphus papa Cathartidae CAM FS FE, WR, TP
14 Long-tailed Woodcreeper Deconychura longicauda Furnariidae IS, FS BR, FE, WR
15 Mangrove Hummingbird Amazilia boucardi Trochilidae NE, FS FF, HG
16 Marbled Wood-Quail Odontophorus gujanensis Odontophoridae IS, FS BR, FE, FF, HG, WR, TP
17 Mealy Parrot Amazona farinosa Psittacidae FR, FS All
18 Orange-chinned Parakeet Brotegeris jugularis Psittacidae FR, OA All, escept WR
19 Orange-fronted Parakeet Aratinga canicularis Psittacidae FR, FG HG
20 Ornate Hawk-Eagle Spizaetus ornatus Accipitridae CA, FS BR
21 Red-crowned Ant-Tanager Habia rubica Thraupidae IS, FS BR
22 Red-fronted Parakeet Touit costaricensis Psittacidae FR, FS FF
23 Red-lored Parrot Amazona autumnalis Psittacidae FR, FS All
24 Scarlet Macaw Ara macao Psittacidae FR, FS HG, TP, VI
25 Speckled Mourner Laniocera rufescens Incertae Sedis IS, FS BR, WR
26 Three-wattled Bellbird Procnias tricarunculatus Cotingidae FR, FS FE, WR
27 Turquoise Cotinga Cotinga ridgwayi Cotingidae FR, FS HG
28 Wedge-tailed Grass-Finch Emberizoides herbicola Emberizidae GR, OA OP
29 White-crowned Parrot Pionus senilis Psittacidae FR, FG All
30 White-throated Shrike-Tanager Lanio leucothorax Thraupidae IS, FS WR, FE, BR
31 Yellow-billed Cotinga Carpodectes antoniae Cotingidae FR, FS ASP
32 Yellow-tailed Oriole Icterus mesomelas Icteridae IS, FG OP
Guilds: FR = forest specialist, FG = generalist, OA = open area species, FR = Frugivorous, IS = Insectivorous, NE = nectarivorous, CA = Carnivore

169
Table 5.2 Endemic bird species found in the Path of the Tapir Biological Corridor

Common Name Species Family Guild Land-use Found Geographic Range


1 Baird's Trogon Trogon bairdii Trogonidae FR,FS BR,FE,FF,HG,WR,TP Costa Rica - Western Panama
2 Black-bellied Wren Thryothorus fasciatoventris Troglodytidae IS,FS BR,FE,FF,RT Costa Rica - Western Colombia
3 Black-hooded Antshrike Thamnophilus bridgesi Thamnophilidae IS,FS All, except ASP Costa Rica - Western Panama
4 Charming Hummingbird Amazilia decora Trochilidae NE,FG FE, FF, HG, WR, RT Costa Rica - Western Panama
5 Cherries Tanager Ramphocelus costaricensis Thraupidae FR,FG All, except BR, WR Costa Rica - Western Panama
6 Crimson-fronted Parakeet Aratinga finschi Psittacidae FR,OA All Southern Nicaragua - Western Panama
7 Garden Emerald Chlorostilbon assimilis Trochilidae NE,FG FF,HG,OP,ASP,RT,VI Costa Rica and Panama
8 Golden-naped Woodpecker Melanerpes chrysauchen Picidae IS,FS All, except VI Costa Rica - Western Panama
9 Hoffmann's Woodpecker Melanerpes hoffmannii Picidae IS,FG FF,HG,OP,ASP,RT,TP Southern Honduras - Costa Rica
10 Mangrove Hummingbird Amazilia boucardi Trochilidae NE,FS FF, HG Costa Rica Pacific Mangrove Forests
11 Orange-collared Manakin Manacus aurantiacus Pipridae FR,FS BR,FE,FF,ASP,WR,TP Costa Rica - Western Panama
12 Riverside Wren Thryothorus semibadius Troglodytidae IS,FS All Costa Rica - Western Panama
13 Rufous-winged Woodpecker Piculus simplex Picidae IS,FS BR, WR Eastern Honduras - Western Panama
14 Scintillant Hummingbird Selasphorus scintilla Trochilidae NE,FG RT Costa Rica - Western Panama
15 Snowy-bellied Hummingbird Amazilia edward Trichilidae NE,FS FE Costa Rica and Panama
16 Spot-crowned Euphonia Euphonia imitans Fringillidae FR,FS All, except OP,ASP,VI Costa Rica - Western Panama
17 Three-wattled Bellbird Procnias tricarunculatus Cotingidae FR,FS FE, WR Eastern Honduras - Western Panama
18 Turquoise Cotinga Cotinga ridgwayi Cotingidae FR,FS HG Costa Rica - Western Panama
19 White-crested Coquette Lophornis adorabilis Trochilidae NE,FG Generalist Costa Rica - Western Panama
20 White-throated shrike-tanager Lanio leucothorax Thraupidae IS,FS BR, FE, WR Eastern Honduras - Western Panama
21 Yellow-billed Cotinga Carpodectes antoniae Cotingidae FR,FS ASP Costa Rica - Western Panama
22 Yellow-crowned Euphonia Euphonia luteicapilla Fringillidae IS,OA All, except BR, WR Nicaragua - Panama
Guilds: FR = forest specialist, FG = generalist, OA = open area species, FR = Frugivorous, IS = Insectivorous, NE = nectarivorous
BR = Biological Reserves, FE = Forest Edges, FF = Forest Fallows, HG = Homegardens, OP = Oil palm, ASP = Agrosilvopastoral systems, WR = Wildlife Refuges, RT =
Residential Tourism Projects, TP = Tree Plantations, VI = Villages

170
Figure 5.1 Bird abundance by census (N = 12) of endangered and threatened species

found in the Path of the Tapir Biological Corridor. Different letters indicate

statistical differences at α = 0.05. Statistical analysis was performed to log

transformed of means.

171
Figure 5.2 Bird abundance by census (N = 12) of endemic species found in the Path

of the Tapir Biological Corridor. Different letters indicate statistical differences at

α = 0.05. Statistical analysis was performed to log transformed of means.

172
Frugivore Insectivore Nectarivore Carnivore Granivore
100%

80%
Relative abundance of species

60%

40%

20%

0%
Endemic species Threatened species
Birds
Figure 5.3. Relative abundance of endemic and threatened bird species (percentage

of species) by habitat guilds found in the Path of the Tapir Biological Corridor,

Costa Rica

173
Forest Specialist Forest Generalist Open Area

100%
Relative abundance of species

80%

60%

40%

20%

0%
Endemic Species Threatened Species
Birds

Figure 5.4 Relative abundance of endemic and threatened bird species (percentage

of species) by feeding guilds found in the Path of the Tapir Biological Corridor,

Costa Rica

174
sp28
sp32

OP
0.5

sp31

ASP
NMDS2

sp4 sp2
sp6
sp10
sp25 WR
sp20sp30
sp21sp11
sp5
sp14
sp26 BR sp8sp18
0.0

sp12 TP
sp13 sp9 sp29
sp17 RT
FE sp23
sp7 sp1 VI
sp16

sp24 sp3

FF
HG
-0.5

sp22 sp15 sp19


sp27

-1.5 -1.0 -0.5 0.0 0.5 1.0

NMDS1

Figure 5.5. Non-Metric Multidimentional scaling (NMDS) ordination of threatened

and endangered species found in ten land-use types in the Path of the Tapir

Biological Corridor.

BR = Biological Reserves, FE = Forest Edges, FF = Forest Fallows, HG = Homegardens, OP = Oil


palm, ASP = Agrosilvopastoral systems, WR = Wildlife Refuges, RT = Residential Tourism Projects,
TP = Tree Plantations, VI = Villages

175
sp21

0.5

TP
ASP
sp13
BR
sp20 sp1 sp11 sp9

sp8 sp6 sp22


sp3 OP
WR
0.0

sp16 sp12 RT sp14


sp5
VI
NMDS2

sp17
sp7
FE FF
sp2

sp19
sp15 sp4
-0.5

HG

sp10
-1.0

sp18

-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5

NMDS1

Figure 5.6. Non-Metric Multidimentional scaling (NMDS) ordination for endemic

species found in ten land-use types in the Path of the Tapir Biological Corridor.

BR = Biological Reserves, FE = Forest Edges, FF = Forest Fallows, HG = Homegardens, OP = Oil


palm, ASP = Agrosilvopastoral systems, WR = Wildlife Refuges, RT = Residential Tourism Projects,
TP = Tree Plantations, VI = Villages

176
Summary and Conclusions

Bird species diversity in ten different land-use types in the Path of the Tapir

Biological Corridor, Costa Rica was studied. The ten land-use types were wildlife

refuges, biological reserves, tree plantations, forest fallows, forest edges, villages,

residential tourism projects, homegardens, agrosilvopastoral systems, and oil palm

plantations. The interest was determining how important the ten different habitat types

were for maintaining the bird diversity of the corridor and how these land uses can be

managed to enhance their conservation value. To address these questions 20 point counts

for each habitat type were used. Bird surveys were carried out over a two-year period

(2008-2009). Each point was surveyed three times over the dry and three times over the

rainy periods of each year, 12 visits per point. Total observation time was 400 hours.

Aside from bird identification over a period of 10 minutes in 50-meter radius plots, bird

activities (e.g. foraging, nesting, just moving, perching) and microhabitat were registered

(e.g. tree, shrub, bush, ground, utility wire, etc).

Overall, a total of 44,917 birds from 48 families, and 334 species were found.

Eighty one percent of birds were recorded utilizing forested habitats. However, 77% of

registered birds were found in the human-modified land-use types. At the landscape

level, while homegardens, agrosilvopastoral systems, and villages had the highest bird

abundance, tree plantations had the lowest. Forested habitats (i.e. biological reserves,

wildlife refuges, forest edges) also had low bird density values. Moreover, whereas forest

edges, forest fallows, homegardens, biological reserves, and wildlife refuges were the

sites with the highest species richness and diversity of species, tree plantations,

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residential tourism, oil palm plantations, and villages had the lowest diversity values

within the biological corridor. The latter two were statistically the least diverse sites from

the ten land-use types assessed.

Species composition also varied across the ten habitat types in the corridor.

Biological reserves, wildlife refuges, and forest edges had the most similar assemblage of

species. This may be because these habitats were dominated by primary and old-

secondary forests, having mostly forest-specialist bird species. Also, tree plantations

seemed to share many species with these three habitat types. Agrosilvopastoral systems,

homegardens, residential tourism projects, and oil palm plantations also had similar

assemblage of species because they were dominated by generalist and open area bird

species. In contrast to this high similarity, more open area habitat species (i.e. villages, oil

palm plantations, and residential tourism projects) tended to have the lowest similarity

indexes in relation to forested biological reserves, wildlife refuges, and even forest edges.

When classifying bird species by habitat guild, 44.5% of species were forest

specialists, 38.9% forest generalists, and 16.6% open area specialists. Regarding feeding

guilds, 53.8% of species were classified as insectivores, 21.2% frugivores, 9%

nectarivores, and 8% each for carnivores and granivores. Also, a total of 32 threatened

species and 22 endemic species were identified. Eight of the 22 endemic species were

also under threat, and there were three endangered species registered: Ara macao,

Amazilia boucardi, and Icterus mesomelas. Overall, 64% and 75% of endemic and

threatened species, respectively, were forest-dependent species. Aside from the 46

species that were endangered, threatened, or endemic, there were other species that

should also be considered of conservation concern such as pollinators, seed dispersers,

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insectivores, scavengers, among others, for the environmental services they provide.

From the insectivorous guild, forest understory dwellers are the most sensitive to land-

use change and were the species that were found the least in the human-modified

landscape. But, overall, all forest-dependent species, including 77 species registered in

these land-use types only, should be considered a priority for conservation planning in the

region.

Based on the results from this study, forested habitats seem to be the most

important land-use type for bird species conservation in the Path of the Tapir Biological

Corridor. No statistical difference was found among the four forested reserves regarding

bird species composition and abundance. Rancho La Merced and Hacienda Baru Wildlife

Refuges as well as Oro Verde Biological Reserve and La Cusinga Eco lodge were

selected because of the commitment of the owners to manage these properties in a

sustainable manner. All four reserves were a mixture of primary and secondary forests

surrounded by other land-use types such as agrosilvopastoral systems, homegardens, tree

plantations, and ecotourism development (e.g., trails and cabins), among others. Except

for Oro Verde, all reserves received tourists regularly, but birdwatching tours are offered

at all locations. Birds were sampled mostly in closed-canopy forests as well as along their

edges. There are around 30 other private initiatives and a national park in the PTBC

similar to these four forested private reserves.

Unfortunately, as mentioned throughout the dissertation, all of these reserves are

interspersed between private properties with multiple landowners. Personal experience in

the area illustrated that there are different interests in and goals for landscape

management within the PTBC. Generally, most local people care about the environment

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and they are aware of the negative consequences associated with eliminating forest cover.

However, the minority, who do not really care about the environment also own important

forest fragments or have political power, and are promoting unsustainable development.

Furthermore, a lack of economic incentives, and in some cases negligence and lack of

control by the local and national authorities, are promoting illegal development and land-

use change in these forested habitats. At present, even though local groups and NGOs

such as ASANA have been working to mitigate the illegal development expansion in the

PTBC, it is difficult to control because of a lack of commitment by all stakeholders in the

region. Land-use change from forests to any other human activity, including residential

projects, is prohibited by law in Costa Rica, but the lack of law enforcement plus all

factors described above make it possible all over the country.

Tourism has became one of the most important sources of income in Costa Rica

and in many countries in the tropics, however, exponential and unplanned growth of

many of these projects jeopardize the biodiversity protected in forested landscapes. For

instance, in the Osa County, which encompasses around 40% of the PTBC area,

construction concessions grew 202% from January 2007 to September 2009. At the

current trend, and under the best scenerio, even if forest cover does not reduce drastically,

road and development would further fragment the already fragmented landscape,

affecting the species that require large areas of connected forests to survive. Therefore,

there is a need to adopt sustainable forestry practices to reduce the impacts that

development causes at the landscape level. In addition, there is a need to provide

alternative management opportunities to local people that ensure income as well as

biodiversity conservation, especially of the more sensitive species.

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In Chapter (5), a few alternatives to manage the PTBC as a conservation unit were

proposed based on concepts of sustainable forestry, habitat-dependency of most bird

species, socio-political and economic situation in the corridor, and the existing country

laws. The main goal would be to manage the corridor in a gradation including protected

areas, integrated management areas, and tree plantations. The 30 private reserves are

expected to be the center of conservation in the region, favoring land-use types that

enhance connectivity for wildlife species while providing goods and services to the local

people and the environment, but that also provide habitat to open-area species. Payment

for environmental services, ecotourism, reforestation, environmental education programs,

and private investment, among others, could provide the incentives and infrastructure that

local people need to practice integrated management effectively in the human-dominated

PTBC.

The human-modified land-use types contribute to the high bird diversity of the

PTBC. For instance, more than 77% of bird species in the corridor utilized at least one of

these six land-uses in comparison to 81% found in forested habitats. Forest cover

conservation in reserves and the establishment of tree plantations and agroforestry

systems, especially with native species, could provide many benefits to society in

general. Tropical trees integrating into the landscape as forest reserves, tree plantations or

as part of agroforestry systems (e.g., home gardens, living fences, agrosilvopastoral

systems, improved fallows) can serve diverse economic, social, and ecological functions

that may ultimately help reduce atmospheric CO2 accumulation, restore degraded soils,

protect water sources, protect and enhance biodiversity, contribute to the wood supply,

and improve human welfare.

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I anticipate that the results from this dissertation will inform local stakeholders

about the importance of the corridor as well as the need to adopt sustainable forestry

practices in the region. However, in order to be effective, the decision making process

should incorporate all participants in the corridor, including government institutions (e.g.

Minister of Environment, Minister of Agriculture and Livestock, Minister of Education,

Water Authorities, the National Institute of Electricity), local people and local groups

(e.g. environmental groups such as ASANA, cooperatives, water management groups

(ASADAS), rural development groups), local universities (e.g University of Costa Rica,

Instituto Tecnológico de Costa Rica, CATIE), international organizations working in the

area (e.g. Pitzer College, TNC), tourism sector (e.g hotel’ owners and managers, travel

agencies), and the real estate and development sectors (e.g. Coldwell Bankers, Punta

Dominical, Costa Rica real state).

Finally, this dissertation is only a two-year bird assessment. To successfully

accomplish and assess the PTBC’s conservation goals or lack thereof, long-term

monitoring programs that include not only birds but also other wildlife taxa and plants is

necessary. Also, more commitment from all stakeholders mentioned above is important

to ensure a truly sustainable corridor in the long term.

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APPENDIX 1. Abundance data for 334 bird species found at ten land-use types in the Path of the Tapir Biological Corridor,
Costa Rica

Common name Scientific name BR FE FF HG OP ASP WR RT TP VI


Accipitridae
Bicolored Hawk Accipiter bicolor 0 1 0 0 0 0 0 0 0 0
Black-Hawk Eagle Spizaetus tyrannus 0 0 0 0 0 0 1 0 0 0
Broad-winged Hawk Buteo platypterus 3 5 0 0 0 0 5 2 0 0
Double-toothed Kite Harpagus bidentatus 6 6 0 0 0 0 13 0 0 0
Gray Hawk Buteo nitidus 0 2 0 0 0 3 0 1 0 0
Gray-headed Kite Leptodon cayanensis 0 1 0 0 0 0 1 0 1 0
Great Black-Hawk Buteogallus urubitinga 2 0 0 0 0 0 3 0 0 0
Mangrove Hawk Buteogallus subtiles 1 1 0 0 0 0 1 0 0 0
Ornate Hawk-Eagle Spizaetus ornatus 1 0 0 0 0 0 0 0 0 0
Osprey Pandion haliaetus 0 0 0 0 0 0 0 0 0 3
Pearl Kite Gampsonyx swainsonii 0 0 0 0 0 3 0 0 0 0
Plumbeous Kite Ictinia plumbea 0 0 0 0 0 0 0 1 0 0
Roadside Hawk Buteo magnirostris 1 6 49 32 63 73 1 43 73 24
Swallow-tailed Kite Elanoides forficatus 4 2 0 1 0 0 0 0 0 0
White Hawk Leucopternis albicollis 4 2 1 0 0 0 3 0 0 0
Alcedinidea
Amazon Kingfisher Chloroceryle amazona 0 1 0 0 0 0 0 0 0 1
Belted Kingfisher Ceryle alcyon 0 0 1 0 0 0 0 0 0 0
Green Kingfisher Chloroceryle americana 0 4 0 0 1 1 0 0 0 0
Ringed Kingfisher Ceryle torquatus 0 0 1 0 0 0 0 0 0 1
Anatidae
Black-bellied Whistling-Duck Dendrocygna autumnalis 0 0 0 2 61 6 0 0 0 4
Apodidae
Costa Rican Swift Chaetura fumosa 0 0 0 0 0 0 0 0 0 1
Lesser Swallow-tailed Swift Panyptila cayennensis 0 0 0 0 0 0 0 0 0 6
Ardeidae
Bare-throated Tiger-Heron Tigrisoma mexicanum 0 0 0 0 0 4 1 0 0 2
Cattle Egret Bubulcus ibis 0 0 0 13 62 316 0 29 5 12

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Fasciated Tiger-Heron Trigrisoma fasciatum 0 0 0 0 0 1 1 0 0 0
Great Egret Ardea alba 0 0 0 1 3 20 0 0 0 0
Green Heron Butorides virescens 0 0 0 0 4 10 0 0 0 2
Little Blue Heron Egretta caerulea 0 0 0 0 2 5 0 0 0 0
Snowy Egret Egretta thula 0 0 0 0 3 17 0 0 0 1
Bucconidae
White-necked Puffbird Notharchus macrorhynchos 3 13 3 3 0 3 6 1 2 0
White-whiskered Puffbird Malacoptica panamensis 2 3 0 0 0 0 3 0 0 0
Caprimulgidae
Common Pauraque Nyctidromus albicollis 1 0 3 0 0 1 2 0 4 0
Cardinalidae
Blue-black Grosbeak Cyanocompsa cyanoides 20 36 50 9 4 15 17 18 18 5
Buff-throated Saltator Saltator maximus 10 31 62 46 0 37 1 30 14 7
Dickcissel Spiza americana 0 0 0 0 0 1 0 0 0 0
Indigo Bunting Passerina cyanea 0 0 1 1 0 0 0 0 0 0
Painted Bunting Passerina ciris 0 0 1 1 0 0 0 0 0 0
Rose-breasted Grosbeak Pheucticus ludovicianus 0 1 3 0 0 2 0 0 0 0
Streaked Saltator Saltator striatipectus 0 0 1 0 0 1 0 0 0 0
Cathartidae
Black Vulture Coragyps atratus 0 2 0 15 9 42 2 9 5 54
King Vulture Sarcoramphus papa 0 7 0 0 0 0 1 0 1 0
Turkey Vulture Cathartes aura 2 7 1 1 11 5 6 1 5 40
Charadriidae
Southern Lapwing Vanellus chilensis 0 0 0 1 0 0 0 0 0 0
Columbidae
Band-tailed Pigeon Patagioenas fasciata 0 0 0 0 0 7 20 0 0 0
Blue Ground-Dove Claravis pretiosa 2 3 4 1 0 1 3 2 0 0
Gray-chested Dove Leptotila cassini 21 26 22 17 6 6 10 6 14 18
Gray-headed Dove Leptotila plumbeiceps 4 5 2 0 0 0 5 0 0 0
Inca Dove Columbina inca 0 0 0 19 9 49 0 12 1 41
Pale-vented Pigeon Patagioenas cayennensis 0 4 8 116 12 34 0 29 1 125
Plain-breasted Ground-Dove Columbina minuta 0 0 0 9 0 0 0 0 0 9

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Red-billed Pigeon Patagioenas flavirostris 0 0 0 3 0 1 1 0 0 0
Rock Pigeon Columba livia 0 0 0 0 0 2 0 0 0 30
Ruddy Quail-Dove Geotrygon montana 9 5 2 0 0 0 13 0 0 0
Ruddy-ground Dove Columbina talpacoti 0 0 35 238 232 185 0 94 2 154
Scaled Pigeon Patagioenas speciosa 1 0 5 12 0 4 0 2 0 0
Short-billed Pigeon Patagioenas nigrirostris 142 125 72 35 21 44 138 58 34 2
White-tipped Dove Leptotila verreauxi 4 35 192 105 83 101 10 111 64 29
Corvidae
Brown Jay Cyanolyca cucullata 2 21 24 26 45 122 2 30 47 12
White-throated Magpie-Jay Calocitta formosa 0 0 0 9 11 0 0 0 6 0
Cotingidae
Three-wattled Bellbird Procnias tricarunculatus 0 2 0 0 0 0 4 0 0 0
Turquoise Cotinga Cotinga ridgwayi 0 0 0 1 0 0 0 0 0 0
Yellow-billed Cotinga Carpodectes antoniae 0 0 0 0 0 1 0 0 0 0
Cracidae
Crested Guan Penelope purpurascens 12 0 0 0 0 0 20 0 0 0
Gray-headed Chachalaca Ortalis cinereiceps 2 5 74 55 0 24 0 50 0 7
Great Curassow Crax rubra 30 5 0 0 0 0 42 0 0 0
Cuculidae
Groove-billed Ani Crotophaga sulcirostris 0 0 0 13 145 20 0 14 3 6
Mangrove Cuckoo Coccyzus minor 0 1 0 2 2 3 1 1 1 0
Pheasant Cuckoo Dromococcyx phasianellus 0 1 0 0 0 0 0 0 0 0
Smooth-billed Ani Crotophaga ani 0 0 3 37 49 86 0 44 2 57
Squirrel Cuckoo Piaya cayana 2 10 2 2 0 5 1 0 0 0
Striped Cuckoo Tapera naevia 0 2 2 7 13 9 0 0 0 0
Emberizidae
Black-striped Sparrow Arremonops rufivirgatus 3 7 136 52 140 153 0 56 17 16
Blue-black Grassquit Volantinia jacarina 0 4 96 108 333 431 0 152 11 104
Orange-billed Sparrow Arremon aurantiirostris 27 16 6 0 0 0 17 0 6 0
Ruddy-breasted Seedeater Sporophila minuta 0 0 3 0 9 5 0 0 0 2
Slate-colored Seedeater Sporophila schistacea 0 0 0 0 1 1 0 0 0 0
Stripe-headed Brush-Finch Buarremon torquatus 2 0 0 0 0 0 0 0 0 0

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Stripe-headed Sparrow Aimophila ruficauda 0 0 0 0 4 0 0 0 0 0
Thick-billed Seed-Finch Oryzoborus funereus 0 0 9 7 32 48 0 6 0 2
Variable Seedeater Sporophila americana 0 0 124 248 350 362 0 160 17 194
Wedge-tailed Grass-Finch Emberizoides herbicola 0 0 0 0 3 0 0 0 0 0
White-collared Seedeater Sporophila torqueola 0 0 2 14 45 17 0 3 0 5
Yellow-bellied Seedeater Sporophila nigricollis 0 0 3 3 4 3 0 0 0 1
Yellow-faced Grassquit Tiaris olivaceus 0 0 5 3 3 37 0 15 0 0
Falconidae
Barred Forest-Falcon Micrastur ruficollis 0 0 0 0 0 0 2 0 0 0
Bat Falcon Falco rufigularis 0 0 0 1 0 3 0 0 0 0
Collared Forest-Falcon Micrastur semitorquatus 2 1 0 0 0 0 6 0 0 0
Crested Caracara Caracara cheriway 0 0 0 1 19 14 0 4 4 3
Laughing Falcon Herpetotheres cachinnans 2 8 7 4 7 0 11 3 5 1
Yellow-headed Caracara Milvago chimachima 0 0 4 13 13 24 0 3 6 13
Formicariidae
Black-faced Antthrush Formicarius analis 7 3 0 0 0 0 8 0 0 0
Streak-chested Antpitta Hylopezus perspicillatus 5 1 0 0 0 0 13 0 0 0
Fringillidae
Spot-crowned Euphonia Euphonia imitans 26 20 9 7 0 0 36 4 6 0
Thick-billed Euphonia Euphonia laniirostris 0 14 9 28 13 5 0 10 4 16
White-vented Euphonia Euphonia minuta 5 6 0 0 0 0 2 0 0 0
Yellow-crowned Euphonia Euphonia luteicapilla 0 19 41 94 94 163 6 80 93 159
Yellow-throated Euphonia Euphonia hirundinacea 0 8 23 36 35 18 2 23 16 12
Furnariidae
Black-striped Woodcreeper Xiphorhynchus lachrymosus 19 12 0 0 0 0 25 0 4 0
Buff-throated Foliage-gleaner Automolus ochrolaemus 3 0 0 0 0 0 7 0 0 0
Cocoa Woodcreeper Xiphorhynchus susurrans 59 74 55 35 24 19 77 16 47 0
Long-tailed Woodcreeper Deconychura longicauda 2 1 0 0 0 0 3 0 0 0
Northern Barred-Woodcreeper Dendrocolaptes sanctithomae 14 10 5 0 0 0 22 0 1 0
Olivaceous Woodcreeper Sittasomus grisicapillus 0 0 0 0 0 0 0 0 1 0
Pale-breasted Spinetail Synallaxis albescens 0 0 0 0 2 53 0 1 0 0
Plain Xenops Xenops minutus 18 9 12 10 0 6 26 8 18 0

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Ruddy Woodcreeper Dendrocincla homochroa 3 1 0 0 0 0 1 0 0 0
Scaly-throated Leaftosser Sclerurus guatemalensis 5 0 0 0 0 0 2 0 0 0
Slaty Spinetail Synallaxis brachyura 0 1 11 0 0 5 0 0 0 0
Spotted Woodcreeper Xiphorhynchus erythropygius 1 1 1 0 0 0 0 0 0 0
Streak-headed Woodcreeper Lepidocolaptes souleyetii 1 4 12 28 12 29 0 14 29 9
Striped Woodhaunter Hyloctistes subulatus 1 0 0 0 0 0 0 0 0 0
Tawny-winged Woodcreeper Dendrocincla anabatina 7 7 2 1 0 0 10 0 9 0
Wedge-billed Woodcreeper Glyphorhynchus spirurus 66 39 5 0 0 0 50 0 19 0
Galbulidae
Rufous-tailed Jacamar Galbula ruficauda 0 1 0 0 0 0 0 0 0 0
Hirundinidae
Bank Swallow Riparia riparia 0 0 0 0 3 0 0 1 0 7
Barn Swallow Hirundo rustica 0 0 0 1 0 0 0 0 0 0
Blue-and-white Swallow Pygochelidon cyanoleuca 0 0 0 2 0 13 0 0 0 0
Brown-chested Martin Progne tapera 0 0 0 0 0 0 0 0 0 7
Gray-breasted Martin Progne chalybea 0 0 0 3 15 5 0 1 0 23
Northern Rough-winged
Swallow Stelgidopteryx serripennis 0 0 0 8 21 13 0 2 0 22
Southern Rough-winged
Swallow Stelgidopteryx ruficolis 0 0 0 18 41 38 0 7 0 23
Icteridae
Baltimore Oriole Icterus galbula 0 3 20 31 20 30 0 16 18 26
Black-cowled Oriole Icterus prosthemelas 0 1 0 1 5 1 0 0 0 0
Bronzed Cowbird Molothrus aeneus 0 0 0 9 39 41 0 0 0 3
Eastern Meadowlark Sturnella magna 0 0 0 0 0 2 0 0 0 0
Giant Cowbird Molothrus oryzivorus 0 0 0 0 2 1 0 0 0 0
Great-tailed Grackle Quiscalus mexicanus 0 0 1 350 160 183 0 52 13 985
Melodious Blackbird Dives dives 0 0 1 88 9 45 0 7 1 61
Orchard Oriole Icterus spurius 0 3 0 7 1 0 0 1 0 1
Red-breasted Blackbird Sturnella militaris 0 0 0 0 0 2 0 0 0 0
Scarlet-rumped Cacique Cacicus uropygialis 84 83 38 25 0 2 78 3 53 0
Yellow-billed Cacique Amblycercus holosericeus 0 0 20 0 0 0 0 0 0 0

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Yellow-tailed Oriole Icterus mesomelas 0 0 0 0 1 0 0 0 0 0
Incertae Sedis
Bananaquit Coereba flaveola 0 4 46 70 0 44 0 41 2 30
Black-and-white Becard Pachyramphus albogriseus 2 0 0 0 0 0 0 0 0 0
Black-crowned Tityra Tityra inquisitor 2 12 21 33 13 19 4 10 9 17
Cinnamon Becard Pachyramphus cinnamomeus 0 0 1 0 0 0 0 0 0 0
Masked Tityra Tityra semifasciata 2 22 11 28 3 15 5 5 10 12
Rose-throated Becard Pachyramphus aglaiae 1 8 4 2 0 1 3 0 7 0
Rufous Piha Lipaugus unirufus 32 23 0 0 0 0 49 0 1 0
Speckled Mourner Laniocera rufescens 1 0 0 0 0 0 1 0 0 0
Thrushlike Schiffornis Schiffornis turdina 12 2 0 0 0 0 6 0 0 0
White-winged Becard Pachyramphus polychopterus 0 3 1 2 0 5 1 0 7 0
Jacanidae
Northern Jacana Jacana spinosa 0 0 0 2 0 33 0 0 0 7
Momotidae
Blue-crowned Motmot Momotus momota 50 58 37 25 0 21 25 17 18 0
Nyctibiidae
Common Potoo Nyctibius griseus 0 0 0 0 0 0 1 0 0 0
Odontophoridae
Marbled Wood-Quail Odontophorus gujanensis 11 11 3 3 0 0 2 0 3 0
Parulidae
American Redstart Setophaga ruticilla 2 1 0 1 0 1 1 0 1 0
Bay-breasted Warbler Dendroica castanea 0 0 1 0 0 0 0 0 0 0
Black-and-white Warbler Mniotilta varia 2 5 2 2 0 1 2 0 2 0
Blue-winged Warbler Vermivora pinus 0 0 0 1 0 0 0 0 0 0
Buff-rumped Warbler Phaeothlypis fulvicauda 18 14 1 1 0 0 3 0 0 1
Cerulean Warbler Dendroica cerulea 0 1 0 0 0 0 0 0 0 0
Chesnut-sided Warbler Dendroica pensylvanica 19 41 65 27 5 40 23 17 71 6
Common Yellowthroat Geothlypis trichas 0 0 0 1 0 2 0 0 0 0
Golden-winged Warbler Vermivora chrysoptera 1 1 1 0 0 0 1 0 0 0
Gray-crowned Yellowthroat Geothlypis poliocephala 0 0 2 0 0 6 0 0 0 0
Hooded Warbler Wilsonia citrina 0 0 0 2 0 0 0 0 0 1

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Kentucky Warbler Oporornis formosus 1 0 4 0 0 0 0 0 1 0
MacGillivray's Warbler Oporornis tolmiei 0 0 0 0 0 1 0 0 0 0
Magnolia Warbler Dendroica magnolia 0 0 0 1 0 0 0 0 0 0
Mourning Warbler Oporornis philadelphia 0 0 5 0 1 4 0 0 1 0
Northern Waterthrush Seiurus noveboracensis 0 3 0 0 2 0 0 0 0 0
Ovenbird Seiurus aurocapilla 0 0 0 0 0 0 2 0 0 0
Prothonotary Warbler Protonotaria citrea 0 0 0 0 0 2 0 0 0 0
Tenessee Warbler Vermivora peregrina 9 20 82 34 25 50 7 27 41 20
Tropical Parula Parula pitiayumi 0 0 0 2 0 0 0 0 0 0
Wilson's Warbler Wilsonia pusilla 0 1 3 1 4 3 1 0 1 2
Worm-eating Warbler Helmitheros vermivorum 1 0 0 0 0 0 0 0 0 0
Yellow Warbler Dendroica petechia 0 1 10 50 68 47 0 19 30 55
Yellow-breasted Chat Icteria virens 0 0 1 0 0 0 0 0 0 0
Yellow-throated Warbler Dendroica dominica 0 0 2 2 0 0 0 0 0 0
Passeridae
House Sparrow Passer domesticus 0 0 0 0 0 0 0 0 0 65
Picidae
Golden-naped Woodpecker Melanerpes chrysauchen 58 68 26 22 3 11 53 16 17 0
Hoffmann's Woodpecker Melanerpes hoffmannii 0 0 1 1 3 1 0 2 2 0
Lineated Woodpecker Dryocopus lineatus 2 12 8 12 13 18 1 5 19 2
Olivaceous Piculet Picumnus olivaceus 0 7 22 13 0 9 5 10 6 0
Pale-billed Woodpecker Campephilus guatemalensis 19 23 1 1 0 0 48 1 1 0
Red-crowned Woodpecker Melanerpes rubricapillus 3 12 92 188 153 225 1 91 116 160
Red-rumped Woodpecker Veniliornis kirkii 1 0 0 0 0 0 2 0 0 0
Rufous-winged Woodpecker Piculus simplex 1 0 0 0 0 0 2 0 0 0
Pipridae
Blue-crowned Manakin Pipra coronata 151 140 23 0 0 0 144 0 27 0
Orange-collared Manakin Manacus aurantiacus 19 14 20 0 0 1 5 0 6 0
Red-capped Manakin Pipra mentalis 56 33 4 2 0 0 45 0 2 0
White-ruffed Manakin Corapipo leucorrhoa 1 0 2 0 0 0 1 0 0 0
Psittacidae
Blue-headed Parrot Pionus menstruus 0 0 0 4 0 0 0 0 0 15

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Brown-hooded Parrot Pionopsitta haematotis 12 15 0 0 0 8 33 0 0 0
Crimson-fronted Parakeet Aratinga finschi 8 11 8 77 10 106 11 16 37 55
Mealy Parrot Amazona farinosa 47 74 4 52 2 8 70 19 7 19
Orange-chinned Parakeet Brotegeris jugularis 4 29 71 194 121 188 0 105 197 287
Orange-fronted Parakeet Aratinga canicularis 0 0 0 4 0 0 0 0 0 0
Red-fronted Parakeet Touit costaricensis 0 0 3 0 0 0 0 0 0 0
Red-lored Parrot Amazona autumnalis 49 37 4 129 2 10 42 53 15 66
Scarlet Macaw Ara macao 0 0 0 50 0 0 0 0 2 64
White-crowned Parrot Pionus senilis 67 103 128 188 34 101 57 59 73 71
Rallidae
Gray-necked Wood-Rail Aramides cajanea 2 5 13 16 36 8 8 2 2 7
Purple Gallinule Porphyrio martinica 0 0 0 0 3 8 0 0 0 10
White-throated Crake Laterallus albigularis 0 0 0 0 0 2 0 0 0 0
Ramphastidae
Chesnut-mandibled Toucan Ramphastos swainsonii 130 206 110 77 12 64 177 114 54 14
Fiery-billed Aracari Pteroglossus frantzii 71 99 57 63 0 43 63 64 39 9
Strigidae
Crested Owl Lophostrix cristata 0 5 0 0 0 0 0 0 0 0
Ferruginous Pygmy-Owl Glaucidium brasilianum 0 0 0 5 0 0 0 0 0 3
Mottled Owl Ciccaba virgata 1 1 0 0 0 0 0 0 0 0
Spectacled Owl Pulsatrix perspicillata 2 0 0 6 0 0 2 0 0 0
Striped Owl Pseudoscops clamator 0 0 0 0 1 0 0 0 0 0
Vermiculated Screech-Owl Megascops guatemalae 0 0 0 0 0 0 1 0 0 0
Sylviidae
Long-billed Gnatwren Ramphocaenus melanurus 46 33 12 0 0 0 50 1 10 0
Tropical Gnatcatcher Polioptila plumbea 8 28 35 14 9 0 10 4 36 0
Thamnophilidae
Bare-crowned Antbird Gymnocichla nudiceps 4 3 0 0 0 0 6 0 0 0
Barred Antshrike Thamnophilus doliatus 2 12 54 19 4 29 0 29 15 1
Bicolored Antbird Gymnopithys leucaspis 3 0 0 0 0 0 6 0 0 0
Black-hooded Antshrike Thamnophilus bridgesi 139 154 120 7 2 0 183 18 54 1
Chesnut-backed Antbird Myrmeciza exsul 202 183 108 13 7 1 292 8 66 0

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Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Dot-winged Antwren Microrhopias quixensis 25 9 2 0 0 0 23 0 0 0
Dusky Antbird Cercomacra tyrannina 14 8 2 0 0 0 12 0 2 0
Great Antshrike Taraba major 0 15 16 1 0 2 0 0 2 0
Plain Antvireo Dysithamnus mentalis 24 5 2 0 0 0 21 0 0 0
Russet Antshrike Thamnistes anabatinus 4 5 0 0 0 0 2 0 0 0
Slaty Antwren Myrmotherula schisticolor 3 1 2 0 0 0 9 0 0 0
Thraupidae
Bay-headed Tanager Tangara gyrola 4 1 12 6 0 5 1 0 0 0
Blue Dacnis Dacnis cayana 0 14 8 14 0 16 2 9 2 7
Blue-gray Tanager Thraupis episcopus 1 3 129 343 80 223 0 202 105 349
Cherries Tanager Ramphocelus costaricensis 0 44 460 445 141 291 0 342 85 332
Golden-hooded Tanager Tangara larvata 25 66 129 98 11 123 9 100 40 57
Gray-headed Tanager Eucometis penicillata 87 81 41 14 0 4 66 0 31 0
Green Honeycreeper Chlorophanes spiza 7 3 7 16 0 2 2 2 1 0
Palm Tanager Thraupis palmarum 0 2 117 288 98 113 0 191 23 269
Red-crowned Ant-Tanager Habia rubica 4 0 0 0 0 0 0 0 0 0
Red-legged Honeycreeper Cyanerpes cyaneus 4 8 19 37 0 23 7 25 6 6
Scarlet Tanager Piranga olivacea 0 2 4 3 2 5 1 0 0 0
Scarlet-thighed Dacnis Dacnis venusta 0 3 3 1 0 0 0 0 0 0
Shining Honeycreeper Cyanerpes lucidus 0 10 11 29 0 3 0 4 1 1
Summer Tanager Piranga rubra 8 16 22 30 6 12 6 6 21 3
Western Tanager Piranga ludoviciana 0 3 0 0 0 0 0 0 0 0
White-lineated Tanager Tachyphonus rufus 0 0 0 0 4 0 0 0 0 0
White-shouldered Tanager Tachyphonus luctuosus 24 1 0 0 0 0 25 0 4 0
White-throated Shrike-Tanager Lanio leucothorax 35 6 0 0 0 0 55 0 0 0
Threskiornithidae
White Ibis Eudocimmus albus 0 0 0 0 0 26 2 0 0 2
Tinamidae
Great Tinamou Tinamus major 33 17 9 0 1 0 46 0 1 0
Little Tinamou Crypturellus soui 14 13 8 1 0 0 25 1 4 0
Trochilidae

191
Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Snowy-bellied Hummingbird Amazilia edward 0 1 0 0 0 0 0 0 0 0
Band-tailed Barbthroat Threnetes ruckeri 7 20 2 1 0 0 9 0 7 0
Blue-tailed Hummingbird Amazilia cyanura 0 0 2 0 0 0 0 0 0 0
Blue-throated Goldentail Hylocharis eliciae 27 38 48 27 14 8 25 16 64 5
Bronzy Hermit Glaucis aeneus 0 19 1 0 0 0 1 0 0 0
Charming Hummingbird Amazilia decora 0 5 4 7 0 0 2 2 0 0
Garden Emerald Chlorostilbon assimilis 0 0 5 13 1 4 0 4 0 5
Green-breasted Mango Anthracothorax prevostii 0 2 0 14 0 1 0 2 0 1
Green-crowned Brilliant Heliodoxa jacuna 1 1 0 0 0 0 0 0 0 0
Long-billed Hermit Phaethornis logirostris 56 37 6 14 1 0 45 1 9 0
Long-billed Starthroat Heliomaster longirostris 0 5 5 5 1 2 0 0 5 0
Mangrove Hummingbird Amazilia boucardi 0 0 1 1 0 0 0 0 0 0
Purple-crowned Fairy Heliothryx barroti 11 20 18 25 1 5 9 20 9 2
Ruby-throated Hummingbird Archilochus colubris 0 0 5 2 0 1 0 0 0 0
Rufous-tailed Hummingbird Amazilia tzacatl 1 8 36 65 15 37 0 49 11 35
Scaly-breasted Hummingbird Phaechroa cuvierii 5 5 10 6 0 2 12 4 5 1
Scintillant Hummingbird Selasphorus scintilla 0 0 0 0 0 0 0 1 0 0
Steely-vented Hummingbird Amazilia saucerrottei 0 1 2 0 0 0 0 0 0 0
Stripe-throated Hermit Phaethornis striigularis 13 30 8 7 0 0 10 3 7 2
Violet Sabrewing Campylopterus hemileucurus 1 2 0 0 0 0 1 0 0 0
Violet-crowned Woodnymph Thalurania colombica 33 25 10 4 0 2 27 4 10 0
Violet-headed Hummingbird Klais guimeti 3 4 0 4 1 1 4 0 2 1
White-crested Coquette Lophornis adorabilis 1 1 2 5 0 0 2 0 0 0
White-necked Jacobin Florisuga mellivora 6 15 21 29 3 11 2 15 10 3
White-tipped Sicklebill Eutoxeres aquila 3 0 0 0 0 0 0 0 0 0
Troglodytidae
Black-bellied Wren Thryothorus fasciatoventris 2 30 13 0 0 0 0 2 0 0
House Wren Troglodytes aedon 0 0 45 308 348 157 0 180 77 254
Plain Wren Thryothorus modestus 0 4 60 73 133 74 0 81 19 39
Riverside Wren Thryothorus semibadius 97 184 95 25 2 5 83 27 25 3
Rufous-breasted Wren Thryothorus rutilus 0 4 0 1 0 0 0 0 0 0

192
Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Rufous-naped Wren Campylorhynchus rufinucha 0 0 0 5 0 2 0 0 0 22
Scaly-breasted Wren Microcerculus marginatus 18 0 0 0 0 0 20 0 0 0
White-breasted Wood-Wren Henicorhina leucosticta 1 0 0 0 0 0 1 0 0 0
Trogonidae
Baird's Trogon Trogon bairdii 12 6 3 1 0 0 5 0 5 0
Black-throated Trogon Trogon rufus 19 18 0 1 0 0 27 0 3 0
Slaty-tailed Trogon Trogon massena 36 30 22 18 0 6 26 6 23 0
Violaceous Trogon Trogon violaceus 7 16 18 10 0 2 5 3 6 0
Turdidae
Clay-colored Robin Turdus grayi 0 11 47 268 21 56 0 94 2 212
Swainson's Thrush Catharus ustulatus 21 43 26 11 1 10 10 11 8 4
White-throated Robin Turdus assimilis 1 0 0 0 0 0 0 0 0 0
Tyrannidae
Acadian Flycatcher Empidonax virescens 0 2 1 0 0 0 1 0 1 0
Alder Flycatcher Empidonax alnorum 0 0 3 0 0 3 0 0 0 0
Black-tailed Flycatcher Myiobius atricaudus 11 11 0 0 0 0 6 0 0 0
Boat-billed Flycatcher Megarhynchus pitangua 3 13 16 34 29 43 4 20 34 26
Bright-rumped Attila Attila spadiceus 22 14 19 17 15 12 14 16 18 6
Common Tody-Flycatcher Todirostrum cinereum 0 0 9 27 3 26 0 11 4 25
Dusky-capped Flycatcher Myiarchus tuberculifer 1 7 3 2 5 4 2 1 14 0
Eastern Wood-Pewee Contopus virens 0 0 0 1 0 12 0 0 1 0
Eye-ringed Flatbill Rhynchocyclus brevirostris 4 0 0 0 0 0 3 0 0 0
Golden-crowned Spadebill Platyrinchus coronatus 18 5 0 0 0 0 38 0 0 0
Gray Kingbird Tyrannus dominicensis 0 0 0 0 1 0 0 0 0 0
Gray-capped Flycatcher Myiozetetes granadensis 1 1 10 37 0 22 0 21 2 39
Great Crested Flycatcher Myiarchus crinitus 8 20 30 21 14 12 11 26 28 3
Great Kiskadee Pitangus sulphuratus 4 9 92 250 214 236 0 168 50 329
Greenish Elaenia Myiopagis viridicata 0 3 3 1 0 0 0 0 0 0
Least Flycatcher Empidonax minimus 0 2 1 0 0 0 0 0 1 0
Lesser Elaenia Elaenia chiriquensis 0 0 0 1 0 4 0 0 0 0
Northern Bentbill Oncostoma cinereigulare 2 2 4 0 0 0 1 1 1 0
Northern-scrub Flycatcher Sublegatus arenarum 0 0 0 0 0 0 0 0 1 0

193
Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Ochre-bellied Flycatcher Mionectes oleagineus 29 24 3 0 0 0 58 0 12 0
Olive-sided Flycatcher Contopus cooperi 1 1 2 1 0 4 0 0 1 0
Paltry Tyrannulet Zimmerius vilissimus 1 5 7 5 2 8 0 9 8 2
Panama Flycatcher Myiarchus panamensis 0 0 1 0 0 0 1 0 0 0
Piratic Flycatcher Legatus leucophaius 56 57 74 144 36 133 35 100 56 124
Royal Flycatcher Onychorhynchus coronatus 0 6 0 0 0 0 0 0 0 0
Ruddy-tailed Flycatcher Terenotriccus erythrurus 9 5 0 0 0 0 18 0 0 0
Rufous Mourner Rhytipterna holerythra 16 8 0 0 0 0 22 0 0 0
Rusty-marginated Flycatcher Myiozetetes cayanensis 0 0 0 0 0 0 0 0 0 2
Scissor-tailed Flycatcher Tyrannus forficatus 0 0 1 2 0 3 0 4 0 0
Slate-headed Tody-Flycatcher Poecilotriccus sylvia 2 0 4 4 0 0 2 0 0 0
Social Flycatcher Myiozetetes similis 0 0 22 95 6 54 0 59 5 111
Southern Beardless-Tyrannulet Camptostoma obsoletum 0 3 8 14 0 5 2 10 4 1
Streaked Flycatcher Myiodynastes maculatus 3 22 20 46 72 58 0 34 99 55
Sulphur-bellied Flycatcher Myiodynastes luterventris 1 2 3 6 0 3 1 0 3 2
Sulphur-rumped Flycatcher Myiobius sulphureipygius 12 1 0 0 0 0 10 0 0 0
Tropical Kingbird Tyrannus melancholicus 0 2 81 237 134 180 0 202 23 261
Tropical Pewee Contopus cinereus 0 1 3 1 0 13 0 0 2 2
Western Kingbird Tyrannus verticalis 0 0 3 9 31 17 0 10 0 8
Western Wood-Pewee Contopus sordidulus 0 1 2 0 0 6 0 0 0 0
White-throated Spadebill Platyrinchus mystaceus 2 0 0 0 0 0 0 0 0 0
Yellow Tyrannulet Capsiempis flaveola 0 1 10 13 16 5 0 3 2 3
Yellow-bellied Elaenia Elaenia flavogaster 0 0 11 71 8 83 0 59 2 28
Yellow-bellied Flycatcher Empidonax flaviventris 2 1 3 2 1 6 2 2 3 1
Yellow-bellied Tyrannulet Ornithion semiflavum 0 4 3 2 0 1 0 1 0 0
Yellow-crowned Tyrannulet Tyrannulus elatus 0 11 1 2 0 4 0 1 1 0
Yellow-olive Flycatcher Tolmomyias sulphurescens 0 10 7 7 3 0 2 2 7 0
Vireonidae
Green Shrike-Vireo Vireolanius pulchellus 5 0 0 0 0 0 6 0 0 0
Lesser Greenlet Hylophilus decurtatus 91 70 45 12 1 5 82 14 40 1
Philadelphia Vireo Vireo philadelphicus 1 8 20 16 4 18 5 13 9 2
Red-eyed Vireo Vireo olivaceus 0 0 0 1 0 3 1 0 0 0

194
Common name Scientific name BR FE FF HG OP ASP WR RT TP VI
Scrub Greenlet Hylophilus flavipes 0 0 0 6 4 1 0 1 0 0
Tawny-crowned Greenlet Hylophilus ochraceiceps 65 13 1 0 0 0 65 0 0 0
Yellow-green Vireo Vireo flavoviridis 0 2 3 2 0 1 0 1 0 0
Yellow-throated Vireo Vireo flavifrons 1 3 5 4 1 5 1 0 3 2

BR = Biological Reserves, FE = Forest Edges, FF = Forest Fallows, HG = Homegardens, OP = Oil palm, ASP = Agrosilvopastoral systems, WR =
Wildlife Refuges, RT = Residential Tourism Projects, TP = Tree Plantations, VI = Villages

195