V

ECOLOGY OF THE BEARDED SCREECH -OWL (MEGASCOPS BARBARUS) IN THE

CENTRAL HIGHLANDS OF CHIAPAS, MEXICO

by

Paula Lidia Enriquez Rocha

B.Sc, Universidad Nacional Autonoma de Mexico, 1990 M.Sc, Universidad Nacional de Costa Rica, 1995

A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENT FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY

in

THE FACULTY OF GRADUATE STUDIES

(Animal Science)

THE UNIVERSITY OF BRITISH COLUMBIA

August 2007

© Paula Lidia Enriquez Rocha, 2007 ABSTRACT

I conducted the first systematic study ever on distribution, abundance, habitat selection, morphology, breeding biology, and diet of the endemic and threatened Bearded Screech-Owl

(Megascops barbarus) in the Central Highlands of Chiapas, Mexico from 2002 to 2004. The

Bearded Screech-Owl was more likely to be detected in moist forests and the average of number of owls detected per linear trail was 1.65±0.61 owls/Km in nine locations. The owl presence appeared to be associated with both moist oak and pine-oak forests at the regional level and at

Huitepec Reserve where there was greatest owl density than reference sites. Within these forest types, canopy cover was the most important measured habitat variable indicating habitat selection of Bearded Screech-Owls. Slope more than 40.3 ± 5.28 % combined with N-NW aspect tended to have higher owl presence, probably because steep slopes with northwest aspect are more humid and also have fewer disturbances by human activities. Estimated mean home range of 8 Bearded Screech-Owls was 22.38 ± 4.21 ha. Mean home range marginally varied between different locations, but was not significantly different between males (N=5) and females (N=3).

Morphological measurements from 39 individuals indicated that this species showed reversed sexual dimorphism, with females being heavier, having longer tail than males, but smaller tarsus and culmen. Moulting occurred in the rainy season (July to October), with the primary and secondary feathers being moulted simultaneously. Subcutaneous fat was moderate to abundant in the dry season only (December to May). The first nest recorded for this species was found in a natural cavity of an old Quercus laurina tree. Four roosting sites were located, two in Clethra macrophylla and two in Pinus ayacahuite. Feces analysis and remains collected in the nest indicated that the Bearded Screech-Owl feeds mostly invertebrates, including Melonontidae

(Coleoptera), and fewer of Orthoptera, Lepidoptera, and Arachnida. Stable isotopes of 513C and .

515N analyzed from body and tail feathers from 24 individuals showed ranges of 3.74%o and

3.99%o respectively, which indicated large variation in the diet among individuals during the period of feather growth. Although there was no significant variation in stable isotopes between sexes, females had wider variation in both isotopes signatures than males. Stable isotopes from feathers ii did not show spatial variation, but using feathers from museum specimens and my field stuffy there were significant differences (P< 0.01) in 515N signature values overtime. This study represents a first step towards our understanding of the ecological requirements of the endemic and threatened Bearded Screech-Owl in the Central Highlands of Chiapas. TABLE OF CONTENTS

ABSTRACT n

TABLE OF CONTENTS iv

LIST OF TABLES vi

LIST OF FIGURES vn

ACKNOWLEDGEMENTS ix

CHAPTER 1: 1 GENERAL INTRODUCTION 1 TROPICAL MONTANE FORESTS IN MESOAMERICA 2 ENDEMIC AND SMALL POPULATIONS : 2 OWL CONSERVATION IN MONTANE FORESTS 4 THE STUDY SPECIES MEGASCOPS BARBARUS (BEARDED SCREECH-OWL) 6 THESIS OBJECTIVES 6 STUDY AREA 7 SURVEY TECHNIQUES 8 OVERVIEW OF THE THESIS 11 REFERENCES 14

CHAPTER 2: 20 DISTRIBUTION AND ABUNDANCE OF THE BEARDED SCREECH-OWL IN THE HIGHLANDS OF CHIAPAS, MEXICO 20 INTRODUCTION 20 METHODS 20 RESULTS 22 DISCUSSION : 23 REFERENCES 31

CHAPTER 3: 33 HOME-RANGE SIZE AND HABITAT ATTRIBUTES ASSOCIATED WITH OCCURRENCE OF THE BEARDED SCREECH-OWL IN CHIAPAS, MEXICO 33 INTRODUCTION 33 STUDY AREA 34 METHODS 36 RESULTS 39 DISCUSSION 41 REFERENCES 60

CHAPTER 4: 66 NATURAL HISTORY OF THE BEARDED SCREECH-OWL IN CHIAPAS 66 INTRODUCTION : 66 STUDY AREA AND METHODS 67 RESULTS •. 69 DISCUSSION 72 REFERENCES 80

iv CHAPTER 5: 84 DIET AND TROPHIC ASSESSMENT OF THE BEARDED SCREECH-OWL USING 513C AND 615N STABLE-ISOTOPES 84 INTRODUCTION 84 METHODS 86 RESULTS 88 DISCUSSION 89 REFERENCES 100

CHAPTER 6: 104 SUMMARY AND CONCLUSIONS 104 BEARDED SCREECH-OWL (ENDEMIC OWL OF TROPICAL MONTANE FORESTS) 104 CONSERVATION ECOLOGY OF THE BEARDED SCREECH -OWL IN THE MONTANE FORESTS OF CHIAPAS 108 FUTURE RESEARCH ON THE BEARDED SCREECH-OWL 109 REFERENCES 110

v LIST OF TABLES

Table 2.1. Sites studied to determine presence of Bearded Screech-Owl in the Central Highlands of Chiapas from 2002-2004. Sites with owl records (*) 25

Table 2.2. Bearded Screech-Owl specimens located in museums and bird collections 26

Table 3.1. Description of the environmental and physiographic habitat variables measured in plots with and without Bearded Screech-Owl detections in the Central Highlands of Chiapas, Mexico 47

Table 3.2. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl. detections in the Central Highlands of Chiapas, Mexico 49

Table 3.3. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected in the Central Highlands of Chiapas, Mexico 50

Table 3.4. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl detections at Huitepec Biological Reserve, San Cristobal de Las Casas, Chiapas, Mexico 51

Table 3.5. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected.at Huitepec Biological Reserve, San Cristobal de las Casas, Chiapas, Mexico 52

Table 3.6. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl detections at El Callejon, San Cristobal de las Casas, Chiapas, Mexico 53

Table 3.7. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected at El Callejon, San Cristobal de las Casas, Chiapas, Mexico 54

Table 3.8. Home-range size of eight adult (AHY) Bearded Screech-Owls in the Central Highlands of Chiapas, Mexico, based on 95% fixed-kernel estimates 55

Table 4.1. Morphological characteristics of captured individuals of the Bearded Screech-Owl in Chiapas. Data shown are mean (±SD; sample size) and range. Mests compared females and males. Bold font represents a significant difference 76

Table 4.2. Invertebrate prey remains found, in 16 feces from 14 Bearded Screech-Owls captured in Chiapas, Mexico 77

Table 5.1. Feathers used from Bearded Screech-Owl specimens located in museums and bird collections 94

vi LIST OF FIGURES

Figure 1.1. The Central Highlands of Chiapas, Mexico. Study area is shown in a black rectangle 13

Figure 2.1. Bearded Screech-Owl distribution in the Central Highlands of Chiapas, Mexico 27

Figure 2.2. Bearded Screech-Owl abundance in nine sites in the Central Highlands of Chiapas, Mexico (total Km surveyed A/= 126 Km) 28

Figure 2.3. Number of Bearded Screech-Owls recorded per Km linear trail and per vegetation type at Huitepec Biological Reserve in 2004. Chiapas, Mexico (total of detections N= 41) 29

Figure 2.4. Detection rates by month and forest type for the Bearded Screech-Owl (owl/Km) in 2004 in the Huitepec Biological Reserve, Chiapas, Mexico 30

Figure 3.1. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Screech-Owl detections in the Central Highlands of Chiapas. Four habitat attributes included in the model were: Canopy cover, diameter at breast height < 5 cm (DBH1), canopy height, and leaf litter depth. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours 56

Figure 3.2. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Screech-Owl in the Huitepec Biological Reserve, San Cristobal de las Casas. Five habitat attributes included in the model were: Canopy cover, diameter at breast height < 5 cm (DBH1), diameter at breast height 16 to 30 cm (DBH3), slope, and distance to permanent water. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours 57

Figure 3.3. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Bearded Screech-Owl in the El Callejon, San Cristobal de las Casas, Chiapas. Four habitat attributes included in the model were: Canopy cover, shrub height, distance to permanent water, and epiphytes. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours 58

Figure 3.4. Box-plots of home range size (ha) of Bearded Screech-owls at El Callejon and Huitepec sites, Central Highlands of Chiapas, Mexico. Boxes represent the 10th and 90th percentiles, the line within each box represents the median, and bars represent 5th and 95th percentiles. F?= 0.495; F1j6 = 5.88, P= 0.051 59

Figure 4.1. Annual cycle of breeding, moulting, and fat accumulation for the Bearded Screech- Owl in the Highlands of Chiapas, Mexico 78

Figure 4.2. Nest of the Bearded Screech-Owl with red-phase female and gray phase nestling in a natural oak cavity in Huitepec Biological Reserve, Chiapas, Mexico. June, 2001. (Photo by Jose Luis Rangel-Salazar) 79

Figure 5.1. Distribution of the stable-nitrogen (15N) and carbon (13C) isotopes values from body feathers (calamus) of the Bearded Screech-Owl. Each point represents an individual owl 95

VII Figure 5.2. a) Carbon isotopes ratios of body and tail feathers from Bearded Screech-Owl [r2- 0.77, P = 0.004). b) Nitrogen isotopes ratios of body and tail feathers from the Bearded Screech- Owl (f= 0.67; P = 0.01) collected in the Central Highlands of Chiapas, Mexico 96

Figure 5.3. Isotopes ratios of 515N (•) and 513C (A) of body feathers from the Bearded Screech- Owl (Megascops barbarus) in nine locations in the Highlands of Chiapas and Guatemala. Locations are in elevation gradient (meters above sea level) from minor to major (range 1000 m), and sample size given in parenthesis. SD values given only for more than one sample 97

Figure 5.4. Annual distribution of the isotope ratios of 513C and 615N of body feathers from Bearded Screech-Owl in the Central Highlands of Chiapas and Guatemala 98

Figure 5.5. a) Isotopes ratios of 613C (%o) and b) Isotopes ratios of 515N (%o) of body feathers from Bearded Screech-Owl per year (1955-2004), as well as one sample from 1897 in the Central Highlands of Chiapas and Guatemala. SD values given for years with more than one sample/yr 99

viii ACKNOWLEDGEMENTS

Many people were involved to this project and made important contributions. First of all, I would like to thank my supervisor Kim Cheng for his kind support and enthusiasm that kept me going. I also would like to thank my committee advisors Peter Arcese, John Elliott, and Ron Ydenberg for their confidence and support in different phases of the project. I am particularly grateful to P. Arcese and J. L. Rangel who advised and assisted me on statistical analyses. J. Ganey and D. Cannings provided critical constructive comments on an earlier draft of Chapters 3 and 4, respectively. For assistance with trapping, banding, tracking owls and habitat measurements, I would like to thank J.L. Rangel, T. Will, A. Licona, E. Pineda, E. Santiz, J. Martinez, M. Hiron, K. Elliott, D. Bradley, J. Gomez, and R. Ruiz. I thank C. Ramirez, C. Pacheco, and M. Giron for insect identification. Marti'nez-lco and H. Castaheda helped me with plant identification. M. Tolksdorf from Monika's Wildlife Shelter in British Columbia taught me how to attach radio-transmitters to owls. R. Powell and E. Naranjo provided me with the Telemetry Programs. Thanks go to E. Valencia (Laboratory of Geographic Information Analysis (LAIGE) at El Colegio de la Frontera Sur (ECOSUR) and A. Licona for assisting me with the geographic data. Thanks to J. T. Marshall Jr. and Steve N. G. Howell for sharing with me their field notes and comments on Bearded Screech-Owls. R. D. Kenner from the Cowan Vertebrate Museum at the University of British Columbia provided the CITES exchange permit. G. Galzi, Laboratory Manager of Faculty of Land and Food Systems at UBC provided technical support for preparing the feather samples. D. Harris at the University of California- Davis' Stable Isotope Facility made stable isotope measurements. To all of them, I am very grateful and I acknowledge their invaluable help. I thank the members of the Asociacion Mexicana Pro Conservacion de la Naturaleza (Pronatura A. C.) Chiapas, for allowing me to conduct part of this research at Huitepec and Moxviquil Reserve. Thanks to the Instituto de Historia Natural de Chiapas (IHNCH) for access to San Jose Ecological Park, F. Lagunas from the Tourist Park Rancho Nuevo (Las Grutas), A. Perez from Laguna Coche, and members of La Florecilla, Albarrada Community (Dos Lagunas), Mercedes-Bazom and El Callejon for access to their properties for conducting part of my research.

I would like to thank M. B. Robbins (University of Kansas Natural History Museum; KUNHM), E. Morales and M. A. Altamirano (Coleccion Zoologica Regional Aves-lnstituto de Historia Natural y Ecologi'a de Chiapas; CZRAV), R. Corado (Western Foundation of Vertebrate Zoology; WFVZ), S. Kenney and P. Sweet (American Museum of Natural History; AMNH) who kindly provided data information and feather samples from specimens deposited in their

ix museums. I thank also D. James (National Museum of Natural History; USNM) and the Royal Ontario Museum (ROM) for providing data information from the skins in their museums. I am grateful to P. Liedo as Director of El Colegio de la Frontera Sur (ECOSUR) for his support in all stages of my studies at UBC. I also thank G. Islebe, M. Gonzalez, M. Rojas, D. Ramos, A. Moron, E. Naranjo, G. Escalona, and C. Lorenzo from ECOSUR for their constant support during my studies. Capturing and banding owls were conducted under permit No. 5127 from Secretarfa de Medioambiente y Recursos Naturales (SEMARNAT). Fieldwork was made possible with logistic and financial support by Latin American Program-Canadian Wildlife Service of Environment Canada, Lincoln Park Zoo, Northwest Habitat Institute-Oregon, El Colegio de la Frontera Sur, and El Consejo Nacional de Ciencia y Tecnologia (CONACyT- Mexico). My graduate study program at UBC has been supported by scholarships from CONACyT (No.119647) and ECOSUR, the C. W. Roberts Jr. Memorial Scholarship from the Faculty of Land and Food Systems, and a University Graduate Fellowship from UBC. I am grateful to my friends in Vancouver including Silvia, Victor, Gigi, Juanita, June, Galina, Katia, Juarez, Tanya, Francisco, Christelle, Brenda and Andre for helping me to feel close to home. Thank you also to my sisters and brothers and all my friends in Mexico, Costa Rica and elsewhere who always gave me their ongoing support and warm feeling. Finally, I would like to dedicate my thesis to the most important people in my life: my partner Jose Luis, my daughters Natalia and Paula, and my parents Bertha and Genaro who have always supported me with enthusiasm, encouragement, and confidence for continuing and accomplishing my goal. Thank you all!

x "It was once widely believed that the voice of owls emanating from the dark forest were an omen of impending ill fortune if not death. Perhaps now we must realize that the increasing absence of owl voices should be taken as an omen of impending ill fortunes for the human species. The future will be a stressful one for owls as well as for all of us!"

(Paul A. Johnsgard 2002).

xi CHAPTER 1:

GENERAL INTRODUCTION

The Neotropical region supports a high avian diversity with 3500 species representing approximately 35.4% of the birds of the world (Stotz et al. 1996). Montane bird species represent a significant component of the Neotropical avifauna. However, tropical montane forests are considered among the world's most threatened ecosystems (Myers et al. 2000, Kappelle and

Brown 2001) because of fragmentation, degradation and the loss of these forests caused by human activities. The landscape transformation is affecting the structure of floristic composition by imposing limiting conditions for many undergrowth shrubs and trees. As a result, the abundance and distribution, as well as the ecological characteristics for many species have changed (Mclntyre 1995). Fragmentation and habitat loss are the most significant threat to wildlife and have also been the most important research issues in conservation biology (Saunders et al.

1991, Caughley and Sinclair 1994).

There is a close relationship between the distribution and the abundance of species.

Species that decline in abundance often decline in the number of sites that they occupy and vice versa (Gaston et al. 2000). Therefore, knowing species distribution, abundance, and habitat use is basic for identifying important areas for conservation. An important topic in ecology to evaluate is the usage an organism makes of its environment, including the kind of food that it eats and the habitat it occupies (Johnson 1980, Kochert 1986). Habitat is defined as a part of the Earth where a species lives temporally or permanently, and habitat choice may eventually determine a species' fate (Krebs 2001). Moreover, as Bibby et al. (2000) have suggested the conservation needs of a particular species can be identified by investigating its pattern of distribution because it will reflect its habitat use. Studying the habitat requirements and use are therefore instrumental to manage and conserve raptors and their habitats (McCallum 1994, Mosher et al. 1987).

1 TROPICAL MONTANE FORESTS IN MESOAMERICA

Tropical montane forest has been defined as middle high elevation, dense, tropical forest with moisture from fog, clouds and rain (Watson and Peterson 1999). The main vegetation in this area consists of cloud forest and humid pine-oak forest. The tropical montane forest in

Mesoamerica includes tropical Mexico and Central America. This region is considered the second most important biodiversity hot spot worldwide (Myers et al. 2000). First, the region is characterized by high R (the accumulation of new species throughout adjacent habitats), but low 3

(the relatively low degree of species overlapping among locations) bird species diversity.

Secondly, the area contains a high number of endemic and threatened avian species (Myers et al. 2000); and thirdly, the area has been under high human pressure (Wagner 1962).

The Mesoamerica tropical montane forests are considered islands because of barriers of dispersal that limit the species distribution (Newton 2003). For this reason, the region is not only considered an Endemic Bird Area (EBA) for the world (Stattersfield et al. 1998), but also a centre of bird speciation because of barriers created by the isolation of mountains (Fjeldsa 1994, Rejinfo et al. 1997, Newton 2003).

The Mesoamerica tropical montane forest has been subjected to habitat loss and fragmentation for a long time (Myers et al. 2000, Kappelle and Brown 2001). Many of these areas have been cleared for urban growth, changes in agriculture techniques, grazing, selective logging for firewood, timber and charcoal, uncontrolled burning, and sand or rock banks (Wagner 1962,

Stattersfield et al. 1999). The region has also been the scene of political conflicts and extreme poverty (Aguilar-Stoen and Dhillion 2003). Today, most of the cloud and humid pine-oak forests are restricted to the steeper, higher, and more remote slopes (Wagner 1962).

ENDEMIC AND SMALL POPULATIONS

The tropical montane forest has an important number of endemic bird species. Endemic species have restricted ranges (i.e. found in specific region and not naturally found anywhere

2 else; Newton 2003) and have been roughly classified as two types: neo-endemics that evolved in situ and were not able to disperse (e.g. species on islands) and paleo-endemics (species that were once widespread but now restricted; Newton 2003). Bird Life International defines a restricted-range species as one that, in historical times, has had an overall range of less than

50,000 km2 (del Hoyo et al. 1999). Species with restricted distribution and small populations are highly vulnerable and sensitive to habitat perturbation or any forms of human pressure. They therefore face severe threats and their populations may become extirpated or even extinct in a short time (Balmford and Long 1994, Renjifo et al. 1997, Watson and Peterson 1999, Kerr and

Burkey 2002). Those species should have high priority in conservation strategies (Balmford and

Long 1994).

Caughley (1994) described two paradigms in conservation biology: the small-populations paradigm that focuses on understanding how low levels of abundance influence population survival, and the declining-population paradigm that attempts to understand how and why populations decline, and tries to design recovery and management plans. Understanding ecological requirements for species survival and how species may adapt to environmental change is fundamental to studying life history traits (i.e. traits associated with vital rates such as growth, survival, and reproduction) in birds (Krebs 2001, Bennett and Owens 2002). In a regional scale, variation in life history and behavioural strategies of populations are the outcome of evolutionary processes that depend on the fitness of particular strategies under predominant environmental conditions (Sterarns 1980). Although there is poor knowledge on life history strategies of many tropical montane bird species (Ricklefs 2000), most of the known bird species from montane tropical ecosystems are characterized by 'slow' life histories (i.e., high survival rates combined with low reproductive rates) that make them more vulnerable to fast environmental changes caused by human activities (Bennett and Owens 2002). Therefore, there is a need for basic life history information on threatened bird species for conservation action.

3 OWL CONSERVATION IN MONTANE FORESTS

Owl studies have permitted the development of both theoretical and applied aspects in conservation biology. These studies have contributed to our understanding on the population limitation in birds, particularly on the role of food as regulatory factor for owl populations (Temple

2001, Newton 2003). Studies have done on population viability analyses (Lande 1988), metapopulation theory (Lande 1987), and the relationship between body size and life history strategies (Western and Ssemakula 1982). Nocturnal raptors are important components of natural communities because they are key predators that limit prey populations and contribute to maintaining prey diversity (Redford 1992). Most of the owl populations have low population densities and are sensitivity to habitat changes. They are therefore considered useful as environmental indicators (Marcot 1995). As indicator species, owls have been useful for protecting ecosystems and designating conservation areas (e.g. Spotted Owl has been used to protect old growth forest ecosystems in the Pacific Northwest of North America; Noon and

McKelvey 1996).

Globally, 195 owl species belonging to the family Strigidae, Order Strigiformes have been described (Konig et al. 1999). Of these, 149 species (76.4%) occur in the tropical areas. Seventy- one species (36%) have been registered in Neotropical region (Konig et al. 1999, Enn'quez et al.

2006). A high number of owl species (77 species) are also associated with mature and old growth forests (Marcot 1995).

Recently, taxonomic studies on mitochondrial DNA have shown that screech owls from

America are Megascops Kaup 1848 and not Otus (Konig et al. 1999, Banks et al. 2003). Based on this classification, 26 Megascops species have been described, 10 of which are found in mountains over 1000 meters above sea level. This is one of the four genera in the family that has better representation in the Neotropical mountains. Seven Megascops are distributed in the

Mesoamerica region and four of them have small geographic ranges, considered endemics with small population sizes (Holt et al. 1999, Konig et al. 1999).

4 Despite the high owl diversity in mountains, they have been poorly studied. For instance, for most of the tropical owl species, only their taxonomy, a short description.on their natural history, and a general description of their distribution exist. Very seldom have their habitats been described (Marcot 1995). The lack of understanding of their biology and ecology has hindered conservation effort for these owl species.

As endemic species are highly vulnerable to extinction, the International Union for the

Conservation of Nature (IUCN; Bird Life International 2004) listed four Megascops as Near- threatened: the Balsas Screech-Owl (Megascops seductus), the Colombian Screech-Owl (M. colombianus), the Cloud-forest Screech-Owl (M. marshalli), and the Bearded Screech-Owl (M. barbarus); the last three species live in montane forests. In Mexico, the Norma Oficial Mexicana

(NOM-059; DOF 2002) listed five Megascops species: one threatened (i.e. Bearded Screech-

Owl) and four under special concern. The Near-threatened species designation refers to species that do not qualify for critically endangered, endangered or vulnerable status, likely to be classified as threatened in the near future pending on more information and a better assessment

(del Hoyo et al. 1999).

There are very few ornithological studies of tropical nocturnal birds, given the difficulty to study them because of their nocturnal behaviour. In most cases their habitat is difficult to access because of dense tropical vegetation. Nevertheless, recently there has been an increase in tropical owl studies. The breeding biology and home range of the Strix (Ciccaba) in Guatemala has been described (Gerhardt et al. 1994), and owl occurrence, habitat use and population density in communities in Costa Rica (Enriquez and Rangel-Salazar 2001), Peru (Lloyd 2003), and Brazil (Borges et al. 2004) have also been examined.

5 THE STUDY SPECIES MEGASCOPS BARBARUS (BEARDED SCREECH-OWL)

Megascops barbarus (Sclater & Salvin) 1868.- (Bearded Screech-Owl, Santa Barbara

Screech-Owl, Bridled Screech-Owl or Tecolote Barbudo). The scientific name of the species

{barbarus) reflects its type location in Santa Barbara, Vera Paz in Guatemala and the owl is not bearded as has been believed (J. T. Marshall, pers comm.). This species belongs to the family

Strigidae (American Ornithologists' Union 1998). The Bearded Screech-Owl is the smallest

Megascops, from 16 to 19 cm in length, and is strictly nocturnal. They are endemic (spatially restricted) to the region from Central Highlands of Chiapas, Mexico (17° 11' N; 92° 53' W), to the

Highlands of Guatemala (15° 00' N; 90° 00'W; Sierra de Los Cuchumatanes, Sierra Chuacus, and Sierra de Las Minas). It lives in the montane cloud and humid oak-pine forests, at elevations from 1 800 to 2 500 m (mostly above 2 000 m) (del Hoyo et al. 1999, Konig et al. 1999). Recently, the species has been listed as threatened on the Mexican Red List (DOF 2002) and near threatened globally (Bird Life International 2004) due to the lack of ecological information (e.g. their nests, eggs, and juveniles have not yet been described; Konig et al. 1999), their restricted distribution, and to the loss of tropical montane forests (Bird Life International 2004). There has not been an evaluation of their population status and the habitat variables that influence their populations. Except for museum skins and accidental records, practically no biological and ecological information is available for this species, thus hindering conservation efforts (Derrickson et al. 1998).

THESIS OBJECTIVES

In this study, I examined the conservation ecology of the Bearded Screech-Owl

(Megascops barbarus) in the Central Highlands of Chiapas, Southern Mexico, a threatened listed species restricted to montane forests.

My objectives were:

6 1) To estimate the distribution and abundance of the Bearded Screech-Owl in the Central

Highlands of Chiapas;

2) To evaluate the home-range size and habitat attributes associated with occurrence.

3) To describe aspects of the natural history in order to better discern the actual conservation status of this endemic owl species with reference to the increasingly fragmented and disappearing tropical montane humid forests.

4) To make a diet and trophic assessment for the Bearded Screech-Owl using 5 13C and

515N stable isotopes.

I conducted this study from 2002 to 2004 in the Central Highlands of Chiapas, Southern

Mexico (Fig. 1.1).

STUDY AREA

The Central Highlands of Chiapas, Southern Mexico (17° 11' N; 92° 53' W) is located from 1 500 to 2 000 m in altitude, and only < 4% is at elevation more than 2 500m (Gonzalez-

Espinosa et al. 1995). The climate is temperate sub-humid with a mean annual temperature of

13° to 15°C. The mean annual precipitation is 1 150 mm (> 80% of the annual rainfall occurs between May and October; Garcia 1988). Nocturnal freezing temperatures may occur from

December to March. The main forest types in the region consist of a wide diversity of pines Pinus

spp and oaks Quercus spp (Rzedowski 1978).

There are several human activities that have been transforming the mountain forest

habitat in the Central Highlands of Chiapas. Those activities are: selective extraction of pines for

local timber production, oaks for fuel wood and charcoal, temporal and permanent conversion of forest to agriculture land, and extensive grazing of sheep and cattle in the forests and on

abandoned agricultural land (De Jong et al. 1999). As a result, the region is a mosaic of fragmented forests that includes patches in different stages of succession or degradation

dominated by secondary habitats and infrequent patches of mature forest (Wagner 1962, Ochoa-

7 Gaona and Gonzalez-Espinosa 2000), with increasing isolation of the remnant late successional forest patches (Quintana-Ascencio et al. 1992). The remaining forested area covers 2 911 km2

(46%), but it has been severely fragmented (Ochoa-Gaona and Gonzalez-Espinosa 2000). The annual deforestation rate in the region has been > 2.7% in the last 30 yrs (Gonzalez-Espinosa et al. 1995, Cayuela et al. 2006).

The effects of habitat disturbance on wildlife species in the Central Highlands of Chiapas are poorly known. Current land-use patterns in the region may affect resources available to birds depending on old-growth forests (Gonzalez-Espinosa et al. 1995). Therefore, studies of endangered species are much needed to facilitate adequate measures of conservation of both populations and habitats protection (Konig et al. 1999).

SURVEY TECHNIQUES

Owls are one of the most difficult groups of birds to study, not only because they are

nocturnal, but also because of their elusive and secretive behaviour. As well, most of them live in forested areas (Marcot 1995). As songs or calls of birds play an important role in defence of territory and mate attraction, surveying owls by broadcasting taped vocalizations of conspecifics

(play back method) along roads increases the contact rates and has been demonstrated to be

more effective than trying to detect them by spontaneous singing without any calling broadcasting

(Johnson et al. 1981, Fuller and Mosher 1987, Mosher et al. 1990). This technique could be the only practical way to detect and count rare species in low densities and inaccessible habitats

(Johnson et al. 1981). The broadcasting technique has been efficient for several owl species such as Eastern Screech-Owl (Megascops asio; Carpenter 1987), Ferruginous Pygmy-Owl

(Glaucidium brasilianum; Proudfoot and Beasom 1996), Tawny Owl (Strix aluco; Redpath 1994,

Zuberogoitia and Campos 1998), Barn Owl (Tyto alba; Zuberogoitia and Campos 1998), and

Little Owl (Athene noctua; Zuberogoitia and Campos 1998). In tropical areas this survey

8 technique has also been useful in increasing owl species detection (Enriquez and Rangel-Salazar

1997).

The survey point sampling period varies among studies, but one standard sampling lasts

10 min: 2 min of silence before broadcasting, 3 min of broadcasting of pre-recorded calls and 5 min of silence to record any answer (Kochert 1986). Vocalizations used for broadcasting should be recorded from the same area where the study will take place for better results of response

(personal obs.). Environmental factors which may influence the rate of response or detection include: rain, wind, temperature, lunar cycles, and weather changes (Ganey 1990, Hardy and

Morrison 2000, Enriquez and Rangel-Salazar 2001).

The broadcasting technique has been shown to be effective in owl population or community distribution studies (e.g. Loyn et al. 2001), owl population census studies

(Zuberogoitia and Campos 1998), and habitat use studies (Proudfoot et al. 1997). However,

Zuberogoitia and Campos (1998) have recommended that broadcasting technique have to be complemented with other methods (such as searching for nest) to obtain more information on owl population ecology.

Surveys to locate active nests are useful not only for identifying breeding areas, population dynamics and habitat use, but also for obtaining natural history information of rare species. Walking through areas may be the most common method for finding raptor nests because it provides more opportunities to search for cavities, roosts, pellets or excreta under trees. However, there are logistic limitations such as the time needed to locate nests effectively, and problems with accessing areas because of vegetation and difficult topography (Fuller and

Mosher1987).

Another important issue in raptor studies is food habits, not only in terms of prey items, but also in terms of foraging habits (when and where are they foraging; Marti 1987). Pellet (non digestible regurgitated prey parts) analysis is a common method for determining diet in owls and can provide both qualitative and quantitative information. Pellet analysis offers several

9 advantages over other techniques and has been shown to be effective for medium sized owls

(Marti 1974). However, this technique is not practical for some insectivorous owls because the insects eaten are broken into small fragments and are difficult to identify in the pellets (Marti

1987). Also, some insectivorous owls rarely produce pellets (see Lee and Severinghaus 2004). In addition to pellet analysis, many diet studies are based on direct observations and stomach content analysis, (Marti 1987, Rosenberg and Cooper 1990). The identification of prey items by direct observations is the best technique for those species for which their pellets do not provide good representation of their diets (Marti 1987). However, direct observation is difficult and sometimes not practical for nocturnal species. Analysis of stomach contents requires sacrificing the individual and the quantity of data obtained is minimal compared to other available methods

(e.g. pellets analysis). This invasive technique is also not suitable for rare and endangered species. All the above approaches mentioned may have a variety of logistical and other limitations across species and environments. A more recently developed technique is the analysis of stable isotopes of carbon and nitrogen. Differential fractionation of stable isotopes of carbon

during photosynthesis causes plants C3 and C4to have different carbon-isotopes signatures. The carbon isotope ratio (13C/12C) can be estimated from the consumer's tissues making this technique useful for studying foraging habitat types. The nitrogen isotope (15N) from dietary items is also incorporated into the consumer's tissues and there is an enrichment of nitrogen isotope ratio (15N/14N) with each higher trophic level of the food chain.

Stable isotopes analysis using tissues that are not metabolically active (e.g., feathers) has been a useful tool for studying diets of birds (Mizutani et al. 1990, Thompson and Furness

1995). It is also a good option for studying seasonal and spatial variations of diets for the species of concern. Feathers of little known species collected in different periods of time or locations can

be obtained from museum specimens and other bird (Kelly 2000). One limitation in applying this technique to rare species, however, is the limitation on sample size for obtaining an accurate

estimation of their diet characteristics. However, using conventional dietary measurement

10 methods in combination with stable isotope techniques will imporove our understanding of the trophic ecology of owls.

To study the dispersal, home range (by tracking individuals), morphology, stable

isotopes, toxicology or taxonomy of owls requires that birds be captured for examination,

measurements, tissue samples (blood or feathers) and/or marking. Although there are a wide variety of trapping techniques available for owls, the noose carpet, bal-chatri trap, and mist net

are three main trapping techniques for small owls (Bloom 1987). The noose carpet is a piece of

hardware cloth with monofilament nooses tied to it. It is placed around the branches at perch

sites. The bal-chatri is a wire cage with nooses tied to the top and a live bait animal inside. It is a

very effective trap (Bloom 1987). Mist nets are very successful especially for small sized owls.

Owls can be attracted to the mist- net with lure prey (e.g. mouse) or tape-recording of prey sound

or owl vocalizations. Some owl species are easier to capture and trapping success depends on

factors such as environmental conditions, season of the year, and trap type (Bloom 1987).

OVERVIEW OF THE THESIS

In this introduction chapter, I explained the significance of montane tropical forest for rare

species conservation and the effects of habitat loss for endemic species. Through literature

review I demonstrated the importance of studying the distribution, abundance, habitat use and

natural history traits of bird species to conserv them. I reviewed the limited ecological knowledge

of the Bearded Screech-Owl (Megascops barbarus) to demonstrate the need for more information

about this endemic and threatened species.

In Chapter 2, I explored the spatial distribution of the Bearded Screech-Owl based on

historic and current records from the Central Highlands of Chiapas, Mexico, and presented the

results of my survey of the relative abundance of this species at both regional and local scales.

11 In Chapter 3, I examined which habitat attributes were associated with the presence

(occurrence) of this endemic owl, and evaluate if these habitat attributes and home-range size differed at two sites with different management programs.

In Chapter 4, I evaluated the morphological characteristics, the first nest site, home ranges, roost-sites and diet of the Bearded Screech-Owl in the Central Highlands of Chiapas,

Mexico.

In Chapter 5, I used stable isotopes to analyse whether diet patterns of the Bearded

Screech-Owl varied spatially along the species range in the Central Highlands of Chiapas, and over time.

In Chapter 6, I summarized and discussed my findings and drew conclusions on implications of conservation for this endemic species. I also suggested future research for management and conservation, and made recommendations on the status of Bearded Screech-

Owl in Chiapas, Mexico.

I present Chapters 2, 3, 4, and 5 as manuscripts for publication according to the format of the Journal of Raptor Research.

12 Figure 1.1. The Central Highlands of Chiapas, Mexico. Study area is shown in a black rectangle.

13 REFERENCES

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19 CHAPTER 2:

DISTRIBUTION AND ABUNDANCE OF THE BEARDED SCREECH- OWL IN THE

HIGHLANDS OF CHIAPAS, MEXICO

INTRODUCTION

The Bearded Screech-Owl (Megascops barbarus) is considered a rare species and endemic to the Highlands of Chiapas and Guatemala (pine-oak and cloud forest in elevations of

1800 to 2500 m) and (Holt et al. 1999, Konig et al. 1999). This owl's global conservation status has been classified as near threatened not only because of habitat loss, but also because very little biological information was available for this species (Bird Life International 2004). There are only a few accidental records and a small number of skins in museums. The distribution and abundance of the species has not been systematically documented (Howell and Webb 1995).

Knowledge of distribution patterns and abundance of rare species is crucial for designing conservations strategies and to manage such populations (Mosher and Fuller 1996). Acquiring this information is therefore considered the first step in studying wildlife ecology (Caughley and

Sinclair 1994).

The purpose of this study was to first describe the spatial distribution of the Bearded

Screech-Owl based on historic and current records from the Highlands of Chiapas, Mexico.

Secondly, I surveyed the relative abundance of this species at both regional and local scales.

Information obtained will contribute to identifying important areas and habitats for conservation of this near threatened species.

METHODS

Study Area.-This study was conducted in the Central Highlands of Chiapas, Southern

Mexico (17° 11' N; 92° 53' W) from 1800 to 2500 m elevation. The vegetation includes pine-oak,

20 oak and cloud forests, but also patches of diverse secondary communities associated with pine- oak forests (Rzedowski 1978).

Historical Occurrence.- Information on past occurrence of the Bearded Screech-Owl was obtained from museum collections (Table 2.2), from banding records from a project at the

Huitepec Biological Reserve (Rangel-Salazar and Enriquez 2004), and from personal communications of bird specialists (J. T. Marshall Jr. and S. N. G. Howell).

Current Distribution and Abundance - Current distribution was obtained by a survey study

(2002 - 2004). I selected 15 sampling sites (Table 1) based on habitat type and accessibility to clarify the species' spatial distribution. I used the point-count broadcasting response survey method (Bibby et al. 2000, Gerhardt 1991, Redpath 1994, Enriquez and Rangel-Salazar 2001) to estimate distribution and abundance (Fuller and Mosher 1981). In each sampling site I established a line transect (along trails) with survey stations separated from each other at 0.35

Km intervals. The length of each transect varied according to the terrain conditions (Kockert

1986). The broadcasting survey per station consisted of a 10 minute sampling period that included 2 minutes of silence (to record any owl calling before playback), 3- min sequence of a male call followed by 5 minutes of silence to listen for calling owls. While tapes were running I remained several meters away to minimize my influence (Loyn et al. 2001). When a calling individual was recorded I estimated the owl's position and distance by triangulation (Bell 1964).

Accuracy of this method, however, decreases as distance to the owl increases (Ganey and Balda

1989). I visited each location more than twice. In 2002, the surveys were carried out between

June and December. In 2003, surveys were carried out from January to August, and in 2004, from January to June.

Data Analysis - The relative abundance was estimated by the number of owls calling per

Km surveyed. The total abundance value for the region was the mean number of individuals per location. I obtained population density (D) (owls/ha; Andersen et al. 1985) using the Distance 3.5

21 Program (Thomas et al.1998). Statistical analyses were performed using JMP in SAS 5.1 (Sail et al. 2005). All means are presented (± 1SD) and tests were considered significant at a = 0.05.

All the available data for the bird's occurrence were geo-referenced in ArcView map

(ESRI GIS). Suervey locations without owl records were also mapped (Fig. 2.1).

RESULTS

A total of 30 past Bearded Screech-Owl records were obtained; 16 from museum collections (Table 2.2), 10 from the Huitepec banding project, and four from personal communications. Only three records were from Guatemala. The oldest specimen was collected in

1866 in Alta Vera Paz, Guatemala (USNM 42776). In Mexico the oldest specimen was collected in 1955 in Huixtan, Chiapas (KUNHM 35072), and the most recent previous to this study was in

1999 at Huitepec Biological Reserve (CZRAV 6542).

Spatial Distribution.- Owls were recorded from nine of the 15 sites studied to determine spatial distribution of the Bearded Screech-Owl (Table 2.1), with a total of 54 individuals (14 captured and 40 calling records; Fig. 2.1). The four historic owl occurance sites marked in the Fig.

2.1 were not examined because of inaccessibility or urban development. Most owl occurrences were in moist pine-oak and cloud forests, but also in moist oak forest and a few in pine forests.

The elevation recorded for owl occurrences ranged from 2 134 m at Callejon to 2 698 m at

Tzontehuitz. Most of the historical records were in the highlands of Chiapas; only one owl was collected in 1958 (LACMNH) at El Sumidero, Tuxtla Gutierrez. The maximum elevation in the area was 1 640 m.

Relative Abundance at a regional scale (Landscape).- The mean number of owls detected per Km along linear trails was 1.65+0.61 (nine locations). There were significant

2 differences in the mean number of owls detected Km among locations (X 8= 18.5; P<0.05; Fig.

2.2), but the trails were of various lengths and not standardized. The Huitepec showed the

22 highest owl numbers detected per linear trail (3.37±0.36). The mean density estimated for the study area was 0.025±0.01 owls/Ha.

Relative Abundance at local scale (Huitepec Biological Reserve).- In 2004 the mean number of owls detected per Km along linear trails at Huitepec Biological Reserve was 1.63±0.23 for the moist oak forest and 0.26±0.28 for the cloud forest. However, in the dry oak forest no

Bearded Screech-Owls were recorded. There were differences in the number of detected owls

per linear trail between vegetation types (f10 = 8.51; P<0.0001; Fig. 2.3). But there were no

temporal differences (f5 = 0.54; P<0.99; Fig. 2.4).

DISCUSSION

This study provides the first survey of distribution and abundance of Bearded Screech-

Owl in the Central Highlands of Chiapas. The highlands of Chiapas are characterized by heterogeneous mosaic patches of forest but also cultivated areas. As expected, the Bearded

Screech-Owls were not randomly distributed, but unexpectedly, they seem to be absent from areas that appear to have suitable habitat. I recorded owls only in nine of 15 potentially suitable selected sites and they were more likely to be detected in moist forests. Habitat spatial configuration is said to be the main factor affecting the distribution and abundance of raptor species (Jenkins 1994, Sanchez-Zapata and Calvo 1999). Aside from vegetation type, other factors such as environmental variables such as canopy cover, distance to water, aspect (N-NW), slope, erosion seem to be determinants of its distribution (see Chapter 3), as has been reported for other owl species (Zabel et al. 1995).

The mean number of Bearded Screech-Owls detected was 1.65 owls/Km. Studies on small owls have reported higher densities. For comparison, the endemic Balsas Screech-Owl

(Megascops seductus) in Mexico was 2.5 owls/Km (Alba 2003), and the Northern Pygmy-Owl

(Glaucidium gnoma) in Oregon was 2.24 owls/Km (Sater et al. 2006). The Bearded Screech-Owl

has been considered a rare species (Holt et al. 1999), and my surveys support the IUCN Red

23 List's classification; that the species is rare in some areas and uncommon in others. Another small insectivorous owl with similar density is the Flammulated Owl in New Mexico (0.022 owls/ha; Zwank 1995).

The Huitepec Biological Reserve showed the highest number of owl detections/Km followed by El Callejon. Bearded Screech-Owls at both locations had the most depleted values of stable isotopes of 513C in their feathers, indicating that both locations have mesic habitat conditions (see Chapter 5). At Huitepec, owls were found only in moist oak and cloud forests. The

Bearded Screech-Owl can be considered an obligate forest owl limited primarily to moist forests.

Both types of habitat were different in relative humidity and organic material when compared with successional and incipient forests (Luna 2005). Forest edges were also an important component of habitat selected by Bearded Screech-Owl for roosting sites (see Chapter 4). The detection of owls there suggests that this species may be quite tolerant of habitat alteration by human activities. Selective logging has been carried on in this area and has reduced the heterogeneity of the habitat. The assumption that the density or abundance of a species is a direct measure of habitat quality may be influenced by temporal conditions due to local variation in food availability, predator density, or environmental factors rather than long-term habitat quality (Van Home 1983).

Therefore, long-term studies of survival and reproduction are needed to give us better insight into

Bearded Screech-Owl distribution and abundance.

Although these results provide some information regarding distribution and abundance of the Bearded Screech-Owl, factors that influence their numbers are poorly understood. Therefore, studies are needed on factors that influence population trends (e.g. nest and prey availability) and related mechanisms (e.g. predation) to better predict and identify the effects of forest loss fragmentation on Bearded Screech-Owl populations.

24 Table 2.1. Sites studied to determine presence of the Bearded Screech-Owl in the Central

Highlands of Chiapas from 2002-2004. Sites with owl records (*).

Land Location Altitude Lat/Long Vegetation ownership

Arcotete 2143 16°43'52"N; 92°36'26"W pine-oak forest Public

Florecilla 2300 16°43'00'N; 92°36'20"W pine-oak forest Public

Mercedes-Bazom* 2230 16°48'35"N; 92°34'24"W cloud forest Private

Dos Lagunas* 2500 16°39'28"N; 92°31'11"W pine-oak forest Private

El Callejon* 2197 16°41'24"N; 92°36'10"W pine and pine-oak forest Public

Las Grutas* 2265 16°40'12"N; 92° 35' 05"W pine-oak forest Protected

El Huitepec* 2540 16°45'50"N; 92°40'10"W cloud and oak forests Protected

Lagos Montebello 1500 16°06'45"N; 91°43'35"W pine-oak forest Protected

Laguna Coche* 2180 16°43'39"N; 92°36'43"W pine forest Private

Mitziton* 2482 16°39'41"N; 92°32'37"W pine-oak forest Public

Moxviquil 2241 16°45'22"N; 92°37'55"W oak forest Protected

Yerbabuena 2055 17°11'01"N; 92°53'54"W cloud forest Public

San Jose* 2395 16°40'19"N; 92°42'08"W pine-oak forest Public

Carr. to Tuxtla 2220 16°42'41"N; 92°41'07"W pine-oak forest Public

Tzontehuitz* 2698 16°48'35"N; 92°34'24"W cloud forest Public

25 Table 2.2. Bearded Screech-Owl specimens located in museums and bird collections.

Museum* Date Location Lat/Long No. (sex) Collector KUNHM 3-Mar-55 13.5 Km E to San Cristobal de las Casas, Huixtan 16°43'12"N 92°30'30"W 35072 (0) R. W. Dickerman LACM-NH 15-May-58 Sumidero, Tuxtla Gutierrez Chiapas, Mexico 16°50'40"N 93° 04'35"W 32567 (?) M. Alvarez del Toro WFVZC 14-Oct-62 Finca Patichuitz, 53 Km NE Margaritas, Ocosingo 16°24'35"N 91 °47'45"W 10253 0) A. Gardner LSUMZ 02-Dec-63 Finca Patichuitz, 53 Km NE Margaritas, Ocosingo 16°24'35"N 91°47'45"W 39893(C) A. Gardner CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92° 34'00"W 202(J) M. Alvarez del Toro CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92° 34'00"W 203 (3) M. Alvarez del Toro CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92° 34'00"W 204 (?) M. Alvarez del Toro AMNH 12-Sep-72 8 Km to WNW from San Cristobal, Zinacantan 16°40'05"N 93°42'32"W 6959 (?) J. T. Marshall CZRAV 15-Nov-77 IV) Close to Teopisca, San Cristobal de las Casas 16°31 '00"N 92°28'60"W 205 (<3) Ni** CZRAV 11-Jul-88 Huitepec Biological Station, San Cristobal 16°44'50"N 92°41'10'W 5158 (?) R. Vidal CZRAV Ni** Huitepec Biological Station, San Cristobal 16°44'50"N 92°41'10"W 5171 (S) R. Vidal CZRAV 16-Jul-93 San Jose Bacomtenelte, Zinacantan . 16°43'00"N 92°42'28"W 5513(9) M.A. Altamirano CZRAV 20-Jan-99 Huitepec Biological Station, San Cristobal 16°45'05"N 92°41'00"W 6542(2) J. L. Rangel AMNH May-1897 Baja Vera Paz, Guatemala 14°55'22"N 90°35'26"W 71493 (?) A. Alfaro USNM Oct-1866 Between Coban and Chisec, Alta Vera Paz, Guatemala 15°27'28"N 90°30'25"W 42776 (?) H. Hague USNM 18-Mar-1891 Uspantan-Quiche, Santa Cruz del Quiche.Guatemala 15°03'50"N 91°05'50"W 150916(2) H. T. Heyde

(Th K anS NatUral History Museum ™f f v^niV!rSi!y ? , f ). LACM-NH (Los Angeles California Museum-Natural History), WFVZ (The Western

Z LSUMZ (L Uisiana State Universit fncS, t?H 2 ye,1eMa 6 ?°^}' ° y Museum-Zoology), CZRAV (Coleccion Zoologica Regional deAves History?. " Ni^^Tnrofmation) ChiaPaS)' AMNH (The Amer'Can MUS6Um °f NatUra' HlSt°ry)" USNM (^e National Museum oiNatural Figure 2.1. Bearded Screech-Owl distribution in the Central Highlands of Chiapas, Mexico.

27 4 i 3.5 - 3 - E 2.5 - 2 - g o 1.5 - 1 - 0.5 - 0 -

XT 9>'

Figure 2.2. Bearded Screech-Owl abundance in nine sites in the Central Highlands of Chiapas,

Mexico (total Km surveyed N= 126 Km).

28 2 1.8 1.6 1.4 E 1.2 ^> 1 5 O 0.8 0.6 0.4 0.2 ^ 0 Dry-oak Moist-oak Montane Cloud

Vegetation type

Figure 2.3. Number of Bearded Screech-Owls recorded per Km linear trail and per vegetation type at Huitepec Biological Reserve in 2004. Chiapas, Mexico (total of detections N= 41).

29 Figure 2.4. Detection rates by month and forest type for the Bearded Screech-Owl (owl/Km) in

2004 in the Huitepec Biological Reserve, Chiapas, Mexico.

30 REFERENCES

Alba, Z. A. 2003. Densidad y seleccidn del habitat del Tecolote Ojioscuro del Balsas (Otus seductus) en la Reserva de la Biosfera de Huautla, Morelos. BSc Thesis. Universidad Nacional Autdnoma de Mexico, Mexico. Andersen, D. E., O. J. Rongstard, and W. R. Mytton. 1985. Line transect analysis of raptor abundance along roads. Wildlife Society Bulletin 13: 533-539. Bell, R. E. 1964. A sound triangulation method for counting barred owls. Wilson Bulletin 76: 292-294. Bibby, C. J., N. D. Burgess, D. A. Hill, and S. H. Mustoe. 2000. Bird Census Techniques. Academic Press. Great Britain. Bird Life International. 2004. Megascops barbarus. In IUCN 2006. 2006 IUCN Red List of Threatened Species http://www.iucnredlist.org. Downloaded on 14 September 2006. Caughley, G. and A. R. E. Sinclair. 1994. Wildlife ecology and management. Blackwell Science. Enriquez, P. L. and J. L. Rangel-Salazar. 2001. Owl occurrence and calling behavior in a tropical rain forest. Journal of Raptor Research 35: 107-114. Fuller, M. R. and J. A. Mosher. 1981. Methods of detecting and counting raptors: a review. Pp. 235-246. In C. J. Ralph and J. M. Scott (Eds.). Estimating numbers of terrestrial birds. Studies in Avian Biology No. 6. Allen Press Inc., Lawrence, Kansas, USA. Ganey, J. L. and R. P. Balda. 1989. Distribution and habitat use of Mexican Spotted owls in Arizona. Condor 91: 355-361. Gerhardt, R. P.1991. Response of Mottled Owls (Ciccaba virgata) to broacast of conspecific call. Journal of Field Ornithology 62: 239-244. Holt, D. W., R. Berkley, C. Deppe, P.L. Enriquez, P. D. Olsen, J. L. Petersen, J.L. Rangel, K. P. Segars, and K. L. Wood. 1999. Strigiformes. Pp. 153-242. In J. E del Hoyo, A. Elliott, and J. Sargatal (Eds.). Barn Owls to Hummingbirds. Handbook of the Birds of the World. Vol. 5. Lynx Editions. Barcelona. Spain. Howell, S. and S. Webb.1995. A guide to the birds of Mexico and Northern Central America. London, Oxford University Press. Jenkins A. R. 1994. The influence of habitat on the distribution and abundance of peregrine and lanner falcons in South Africa. Ostrich 65: 281-290. Kochert, M. N. 1986. Raptors. Pp. 313-349. In A. Y. Cooperrider, R. J. Boyd, and H. R. Stuart (Eds.). Inventory and Monitoring of Wildlife habitat. U. S. Department of the Interior. USA.

31 Konig C, F. Weick, and J-H Becking. 1999. Owls. A guide to the owls of the worlds. Yale University Press. Loyn, R. H., E. G. McNabb, L. Volodina, and R. Willing. 2001. Modelling landscape distributions of large forest owls as applied to managing forest in north-east Victoria, Australia. Biological Conservation 97: 361 -376. Luna, C. J. 2005. Distribucion, abundancia y diversidad de Curculionidae (Insecta: Coleoptera) de hojarasca en la Reserva Huitepec, Chiapas, Mexico. MSc Thesis. El Colegio de la Frontera Sur. Chiapas, Mexico. Mosher, J.A. and M.R. Fuller. 1996. Surveying woodland hawks with broadcasts of great horned owl vocalizations. Wildlife Society Bulletin 24: 531-536. Rangel-Salazar, J.L. and P.L. Enriquez. 2004. Ecologfa para la conservacion de comunidades y poblaciones de aves en la Reserva Biologica Cerro Huitepec, Chiapas. El Colegio de la Frontera Sur, Chiapas, Mexico. Technical Report. 17p. Redpath, S. M. 1994. Censusing Tawny Owl Strix aluco by the use of imitation calls. Bird Study 41: 191-198. Rzedowski, J. 1978. Vegetacion de Mexico. Limusa, Mexico, D. F. 432p. Sail, J., L. Creighton, and A. Lehman. 2005. JMP Start Statistics. SAS Institute Inc. 3th Ed. SAS Institute Inc. Thompson Learning, Belmont, California, USA. Sanchez-Zapata, J. A. and J. F. Calvo. 1999. Raptor distribution in relation to landscape composition in semi-arid Mediterranean habitats. Journal of Applied Ecology 36: 254-262. Sater, D. M., E. D. Forsman, F. L. Ramsey, and E. M. Glenn. 2006. Distribution and habitat association of Northern Pygmy-Owls in Oregon. Journal of Raptor Research 40: 89-97. Thomas, L. J.L. Laake, J. F. Derry, S. T. Buckland, D.L. Borchers, D.R. Anderson, K. P. Burnham, S. Strindberg, S. L. Hedley, M. L. Burt, F. Marques, J. H. Pollard, and R. M. Fewster. 1998. Distance 3.5. Research unit for Wildlife Population Assessment, University of St. Andrews, U. K. Van Home, B. 1983. Density as a misleading indicator of habitat quality. Journal of Wildlife Management 74: 893-901. Zwank, P. J. 1995. Density estimates and habitat use by Flammulated Owls in Southern New Mexico. Pp. 475-478. In J. A. Bissonette and P. R. Krausman (Eds.). Integrating people and wildlife for a sustainable future. The Wildlife Society, Bethesda, MD.

32 CHAPTER 3:

HOME-RANGE SIZE AND HABITAT ATTRIBUTES ASSOCIATED WITH OCCURRENCE OF THE

BEARDED SCREECH-OWL IN CHIAPAS, MEXICO

INTRODUCTION

Many temperate forest owls are known to require complex habitats for living, nesting and roosting (Johnsgard 2002). However, the ecology of most tropical forest owls is poorly known and their habitats have seldom been described (Marcot 1995). Identifying the habitat attributes that influence habitat selection and examining how organisms use them to meet their living requirements are essential for understanding the patterns of life history, adaptation and behaviour of species (Johnson 1980, Cody 1985, Block and Brennan 1993). The Bearded Screech-Owl

(Megascops barbarus) is endemic to the Highlands of Chiapas, southern Mexico, and Guatemala

(Konig et al. 1999). This species is restricted to humid pine-oak and cloud forests (Howell and

Webb 1995, del Hoyo et al. 1999), although its habitat use and habitat requirements have not been studied, and little is known of its ecology.

For a long time, the Central Highlands of Chiapas have been exposed to selective logging and the conversion of forest to agriculture, housing, and grazing lands by humans

(Stattersfield et al. 1999, Ochoa-Gaona et al. 2004). Forest conversion affects landscape level patterns of vegetation structure, and can reduce habitat suitability for flora and fauna endemic to the region (Gonzalez-Espinosa et al. 1995, Ochoa-Gaona and Gonzalez-Espinosa 2000). The

Bearded Screech-Owl is listed as a threatened species in Mexico (DOF 2002), and as lower risk/near threatened species globally (Bird Life International 2004) because its distribution is restricted to tropical montane forest which are now declining at increased rates (Ochoa-Gaona and Gonzalez-Espinosa 2000). My objectives in this study were to determine: 1) which habitat attributes are associated with the presence (occurrence) of the endemic Bearded Screech-Owl,

2) whether these attributes differ, specifically in two localities with different management

33 practises, and 3) whether home-range size differs between two areas with different management regimes. My prediction was that different habitat attributes would be associated with the occurrence of this species as have been demonstrated in other forest owl species (e.g. Spotted

Owl [Strix occidentalis]; Ganey et al. 1999, and Western Screech-Owl [Megascops kenicottii];

Rodriguez-Estrella and Pelaez 2003). Temperate forest owls, such as the Mexican Spotted Owl

(S. o. lucida), require complex habitats for long-term persistence (Ganey et al. 1999, Ganey et al.

2005).

I predicted that habitat characteristics such as vegetation type, continuous canopy cover, slope, and close distance to permanent water were correlated to the occurrence of the Bearded

Screech-Owl. High canopy cover has been related to protection against predators and to improved microclimate conditions (Ward era/. 1998). Steep slopes are associasted with to less disturbed areas with better vegetation conditions (Ganey 2004); and close distance to permanent water has been related to moist areas.

STUDY AREA

I conducted this study in the Central Highlands of Chiapas, Southern Mexico (17° 11' N;

92° 53' W). Most of the area is located from 1 500 to 2 000 m in altitude, and only < 4% is at elevation more than 2500m (Gonzalez-Espinosa et al. 1995). The main forest types in this area consist of a wide diversity of pines Pinus spp and oaks Quercus spp (Rzedowski 1978). The vegetation includes also patches of diverse secondary communities associated with pine-oak forest, and montane cloud forests are found on the highest peaks (Wagner 1962). The remaining forested area covers 2 911 km2 (46%) and has been severely fragmented (Ochoa-Gaona and

Gonzalez-Espinosa 2000, Cayuela et al. 2006).

Four main forest types have been described in the region: 1) Cloud forest, moist old growth forest with little perturbation that occurs in isolated patches located in the higher mountains. High humidity and steep slopes characterize this forest type. It has a large number of

34 endemic species including trees, bromeliads, epiphytes and terns. There are usually two or three layers of trees, and a dense shrubby understory. Common trees of the canopy included Abies guatemalensis, Clethra lanata, C. oleoides, Magnolia sharpie, Oreopanax sp., Persea schiedeana, Quercus sp. and others. 2) Oak forest is found in moist areas bordering cloud forests. It may also be little disturbed because of its rugged topography. This type of forest contains mainly oak trees with an understory rich in epiphytes and lianas. Other tree species include Alnus sp., Liquidambar sp., Arbutus xalapensis and scattered pines in the dryer sites. 3)

Pine-oak forest is the most widely distributed vegetation type in the region and contains a mixture of pine and oak trees with a variable understory, usually herbaceous with occasional shrubs and often only low grassy patches between trees. Epiphytes are abundant in areas with continuous canopy, and oaks are more abundant than pines in areas with little disturbance. Some common tree species are: A. xalapensis, Crataegus pubescens, Pinus oocarpa, Quercus crassifolia, Q. rugosa, Q. crispipilis and others. 4) Pine forest is coniferous forest with pines as main tree species. There are two types of pine canopy, one with moderate density and open undergrowth and another with trees widely spaced without undergrowth (called open-pine forest). The open- pine forest occupies the moister region. The vegetation structure is simpler, the soil is compacted, and the understory is practically absent, exposing the forest floor to higher temperatures. The youngest forests have been intensively managed (Breedlove 1973, Rzedowski 1978, Gonzalez-

Espinosa et al. 1997).

To study habitat selection and home range of the Bearded Screech-Owl, I selected two sites that differed in vegetation type, structure, and management: The Cerro Huitepec Biological

Reserve, where the main vegetation type is old growth broadleaf such as oak and cloud forests, and El Callejon, where the main vegetation type is coniferous forest. The Huitepec Biological

Reserve (hereafter Huitepec; 16° 44' 38"N and 92° 40'15"W) is a protected area of 137 ha and located approximately 4.5 km NW of San Cristobal de las Casas. This reserve has very steep slopes, from 40 to 60%, and the altitude ranges from 2 230 to 2 710 m above sea level. The

35 mean annual temperature is 15°C, and the mean annual precipitation is 1300 mm (Ramirez-

Marcial et al. 1988). The main type of vegetation is old growth broadleaf that includes eight

Ouercus species such as Q. laurina, Q. crassifolia and Q. rugosa, as well as Arbutus xalapensis,

Alnus acuminata, Oreopanax xalapensis, Rapanea juergensenii, Clethra macrophylla, Cleyera theaeoides, Persea americana and Styrax argenteus. The cloud forest occurs in the higher parts while scattered pine trees are found in the west part of the reserve (for more details on the vegetation see Ramirez-Marcial et al. 1998). Before the Huitepec became a Biological Reserve in

1987, local people selectively used oak trees by cutting only branches for fuel wood, with the trunks were left uncut. Since the area became a Reserve the vegetation has been recovering, having "dwarf" oaks with big trunks but short height.

El Callejon (16° 41' 47"N and 92° 36' 36"W) is a forest located in a community called

Articulo123 and is approximately 4 km SE of San Cristobal de las Casas. The mean altitude is 2

223 m above sea level, and the mean annual precipitation ranges from 1200 to 1400 mm (Garcia

1988). The main vegetation type is evergreen forest such as pine-oak forest although in some sites pine trees dominate the area. The tree species include Pinus pseudostrobus, P. tecunumani, Quercus crispipilis, Q. rugosa, Crataegus pubescens, and Arbutus xalapensis. The shrubs include Eupatorium ligustrinum, E. mairetianum, Rhus schiedeana, and Baccharis

vaccinioides. Local people have selectively harvested branches or trees for firewood or timber allowing moderate or open undergrowth in the area. People also established trails in the area for walking among communities.

METHODS

Owl sampling.- During the same surveys described in Chapter 2 (Fuller and Mosher

1981, Fuller and Mosher 1987), I surveyed 112 survey points in the Central Highlands of Chiapas to evaluate the habitat attributes that affect the occurance of the Bearded Screech-Owl. At each survey point, I conducted nocturnal broadcasting of edited calls of Bearded Screech-Owls (Ganey

36 and Balda 1989, Proudfoot et al. 1997, Hinam and Duncan 2002, Winton and Leslie 2004).

Vocalizations were of males recorded from the region in which surveys were conducted using a mini-disc (Sony MD-R55) and a Sennheiser (MKE 300) microphone. A 10-min sampling period at each survey point included 2 min of silence to record any owl calling before broadcasting, 3 min of broadcasting of pre-recorded calls followed by 5 min of silence to listen for any owl calling.

While the pre-recorded male calls were broadcast, I remained several meters away to minimize distraction from the broadcasted sound (Loyn et al. 2001). I broadcasted at low volume to ensure that only owls present close to the survey point were recorded (Ganey and Balda 1989,

Rodriguez-Estrella and Pelaez 2003). For the broadcasting surveys, I used the mini-disc and an amplifier power-horn. Surveys were conducted only during periods of low wind and no precipitation.

Habitat sampling.- At a regional level, I sampled habitat attributes at each survey point in circular plots of 0.05 ha (12.62 m radius; James and Shugart 1970, Bibby et al. 2000). At each survey point, I sampled sixteen habitat and eight physiographic attributes suggested by Hays et al. (1981), and Mosher et al. (1987) (Table 3.1).

Radio telemetry sampling.- For estimating home ranges, eight owls were captured with a combined technique using broadcasting of pre-recorded calls and mist-nests at two sites

(Huitepec and El Callejon). Four owls per site were banded with aluminium bands and equipped with cross-chest backpack style radio transmitters (model BD-2G; Holohil System Ltd. Ontario,

Canada). Harnesses were constructed of an elastic band and a reflectance tag was added in the antenna to increase the probability of finding the radio-tagged owls at night. The radio transmitter and harness weighed 1.95g (2.75% and 3.15% of the average body mass of females [mean =

70.71 g; n=11 ] and males [mean= 61.81 g; n=7], respectively). Transmitter battery life was approximately 16 weeks. Radio receiving equipment included an Adcock H-antenna with flexible elements and portable receivers (Telonics Inc. Mesa, AZ, USA). I used Universal Transverse

Mercator (UTM) coordinates for each location that was taken using a "homing method" (visual

37 contact with the animal; Samuel and Fuller 1994) and estimated with a Global Positioning System

(GPS). I located individuals an average of two nights/week with continuous tracking sessions at

20-30-min intervals for 6 hr when weather permitted.

Home ranges of owls were estimated with the Fixed Kernel Home Range Method (95% contour; Worton1989) using the Kernel HR program (Seaman and Powell 1997). Kernel estimators are non-parametric techniques useful for analyzing home range data with respect to space use patterns that provide more precise estimates than many other methods (Seaman et al.

1998). I used vegetation maps to classify vegetation type using a cartographic map (1: 50 000) and confirmed classification on the ground. Thus, I estimated the number of point locations per vegetation type.

Statistical Analyses.- Prior to statistical analysis, data residuals were checked for normality with Shapiro-Wilks (W) test and for equal variance with Bartlet's test (Gotelli and Ellison

2004). Where necessary, data were transformed with square root or arcsine transformations to satisfy parametric assumptions. I performed univariate comparisons for all habitat attributes to determine which attributes differed between survey points with owl presence (detected) and points with absence (non-detected) owls, using chi-square tests for categorical variables and

ANOVA for continuous variables (Zar 1999). For each pair of highly correlated attributes (r> 0.7,

P< 0.05), I selected the variable with the lower univariate P value for inclusion in further statistical analysis.

I used Canonical Analysis of Discriminance (CAD; McGarigal et al. 2000) to separate group of sites with the presence of Bearded Screech-Owls from the group of sites with non- detected owls, and to identify the contribution of selected habitat attributes that better explain group separation. Selected candidate independent attributes were standardized for inclusion in the final model using stepwise selection procedure. Mahalonobis distances (minimum D2) between group centroids were used for maximizing group separation (McGarigal et al. 2000).

Standardized canonical coefficients (d) were obtained for determining correlations of habitat

38 attributes with canonical discriminant functions (McGarigal et al. 2000, Gotelli and Ellison 2004).

Positive canonical coefficients in the discriminant function indicated that an increase in the value of a variable increased the probability that owls would be present at that point. Conversely, a negative canonical coefficient indicated that as the variable values increase, the probability of owl presence decreased (Neter et al. 1996). CAD allowed me to identify a linear combination of covariates, detect significant differences between group centroids and determine individual contribution of covariates to the overall discrimination function (McGarigal et al. 2000).

For testing the relationships between home-range size (ha), study area, and sex, and study area-sex interaction, I used a Generalized Linear Model (GLM-ANOVA). All statistical analyses were performed using JMP in SAS 5.1 (Sail et al. 2005). All means are presented (±

1 SD) and tests were considered significant at a = 0.05.

RESULTS

Habitat association.- Bearded Screech-Owls were documented at 50% of the survey points studied. Mean values of vegetation and physiographic attributes at points with and without documented presence of Bearded Screech-Owls are shown in Table 3.2. The Bearded Screech-

Owl -present points had significantly higher canopy cover, higher density of trees with diameter at breast height (DBH) <5 cm, higher density of trees with DBH between 6 and 15 cm, higher total tree density, higher undergrowth cover, higher leaf litter depth (4.3 cm), less rock cover (6.3 %), different vegetation types, and less erosion (Table 3.2 and 3.3).

Results of the Canonical Analysis of Discriminance (CAD) indicated significant difference

(Wilk's A, u = 0.368, F4,107 = 45.88, P< 0.001) between presence and non-detected points and correctly classified 91 percent of field observations. The four habitat attributes included in the

CAD model (in order of intensity) were percentage of canopy cover (Standardized Canonical

Coefficients, d=1.58), DBH1 (d= 0.72), canopy height (d= -0.47), and leaf litter depth (d=-

0.40). These habitat attributes were strongly correlated with the first canonical discriminant

39 function, producing the largest differences between presence and non-detected survey points of the Bearded Screech-Owl in the region (Fig. 3.1). The degree of erosion, a categorical variable, also was negatively correlated with the presence of the owls (Table 3.3).

Habitat association in two sites.- Mean values of vegetation and physiographic attributes in owl presence and non-detected points for the Huitepec area are showing in Table 3.4 and 3.5.

Bearded Screech-Owl-present points had significantly (or marginally significant) higher canopy cover, and DBH1, less distance to the nearest intermittent water (267 m), and different vegetation

types (Table 3.3). CAD revealed clear differences (Wilk's A, u = 0.225, FSi 24 = 16.51, P < 0.0001) in habitat attributes between presence and non-detected survey points, and correctly classified

93.3 percent of both group points. Habitat attributes included in the model were percent canopy cover (d= 1.16), DBH1 (d= 0.58), DBH3 (d= 0.61), percent slope (d= 0.75), and distance to permanent water (d= -0.95; Fig. 3.2).

At El Callejon, Bearded Screech-Owl -present points had significantly (or marginally significant) higher canopy cover, canopy height, shrub height and ground cover of leaf litter, and lower herb cover and elevation than Bearded Screech-Owl - absent points (Table 3.6 and 3.7).

CAD revealed clear differences (Wilk's A, u = 0.0612, F4t 15 = 57.53, P < 0.0001) in four habitat attributes between Bearded Screech-Owl- present and -absent groups, and correctly classified

100 percent of survey points for both groups. The four habitat attributes included in the model were percent canopy cover (d= 2.89), herb height (d= 0.81), distance to permanent water (d =

0.64), and percentage of epiphytes (d= -0.46) (Fig. 3.3).

Home ranges. - Eight owls were radio tagged and tracked (two males in 2002, and three males and three females in 2004); four of these (3 males and one female) were at Huitepec and four (2 males/females) were at El Callejon. The female at Huitepec was lost to predation away from her home range area. The number of telemetry point locations per owl ranged from 10 to 44.

2 Home-range size was not correlated with the number of locations per owl (R = 0.085; F16 = 0.56;

P= 0.48).

40 Mean home-range size (22.38 ± 4.21 ha; n = 8) for all individuals during the entire monitoring period varied from 4.13 - 36.8 ha. The mean home range recorded for the females was 20.61 ± 6.42 ha (n = 3) and for males was 23.44 ± 6.05 ha (n = 5). The home ranges

between sex there were not different (F1i6 = 0.09; P= 0.07). However, home ranges per sites in the Huitepec tended to be marginally larger than those in El Callejon (30.23 ± 2.96 ha; n = 4;

vs.14.52±5.75 ha; n = 4; F1]6 = 5.88; F= 0.051; Table 3.8; Fig. 3.4).

At Huitepec the owl tracking points were distributed as follows: 70.3% ± 15.92 in moist oak forest, 18.92% ± 6.04 in edges and the female was using cloud forest 10.8%; at El Callejon the tracking points were 83.87% ± 2.52 in pine-oak forest, 4.30% ± 2.35 in edges and 11.82% ±

2.76 in pine forest.

DISCUSSION

Habitat association.- The amount of canopy cover appeared to have a strong influence on habitat selection of Bearded Screech-Owl both at regional and local levels. Other studies on forest owls have demonstrated the importance of canopy cover as a habitat attribute in roosting and nesting sites for the Spotted Owl (Solis and Gutierrez 1990, Ganey and Balda 1994, Ganey et al. 1999), Barred Owl (Hinam and Duncan 2002, Winton and Leslie 2004), Western Screech-

Owl (Rodriguez-Estrella and Pelaez 2003), Flammulated Owl (Zwank 1995), and Balsas

Screech-Owl (Alba 2003). Canopy cover has been related to protection both against predators and adverse weather conditions, as well as providing high prey availability, and better microclimate conditions (Ward et al. 1998, Ganey 2004). In the highlands of Chiapas, canopy cover has been reported as constant throughout the year in the three main forest types in the region (old growth, pine-oak and pine dominated), but decreases from old growth and pine-oak forests to the pine forest (Camacho-Cruz et al. 2000), these changes in canopy cover promote significant changes in the undergrowth composition.

41 Tree density with DBH < 5 cm was another important habitat attribute for the Bearded

Screech-Owl at regional and local level at Huitepec. However, canopy height was a habitat attribute that differed negatively from survey points with and without owl detections in the regional level at Central Highlands of Chiapas. At Huitepec before it became a reserve in 1987, oak trees were selectively logged and branches only were cut for firewood. While the trees were spared and able to regenerate, their growth was dwarfed and most of them remained in the undergrowth

(Ochoa-Gaona and Gonzalez-Espinosa 2000). Thus, harvesting branches for firewood has likely reduced one of the desirable attributes of Bearded Screech-Owl habitat.

Vegetation type appeared be associated with owl presence at the regional level and at

Huitepec. There was higher owl presence in both moist oak and pine-oak forests and those seem to be forest types important for Bearded Screech-Owl in my study areas. Oak trees contributed more to canopy cover than pines, however both oak and pines trees were used by Bearded

Screech-Owl for breeding and roosting, respectively. For example, a Bearded Screech-Owl nest was found in a Quercus laurina (Chapter 4). That oak species is one of the dominant oaks in moist habitats in the Central Highlands of Chiapas (Gonzalez-Espinosa et al. 1995). On the other hand, Pinus ayacahuite was recorded as a roosting site for the Bearded Screech-Owl at Huitepec

(Chapter 4). That pine species has been found in more moist areas together with P. tecunumanii

(Gonzalez-Espinosa et al. 1995). In general, moist areas provide better habitat for survival and reproduction, as reported for the Mexican Spotted Owl (Ganey et al. 2005).

At Huitepec, percent slope was associated with the presence of Bearded Screech-Owl.

Steep slopes (40.34% ± 5.28) in the region are less disturbed from human actions and may retain better vegetation conditions. Slopes of 38.5% (± 5.5) have been reported to be important for nesting sites of the Mexican Spotted Owl (Ganey 2004), and 30.4% (± 14.5) for breeding sites of the Flammulated Owl in New Mexico (Zwank 1995). Slopes with N-NW aspect tended to have more Bearded Screech-Owl records. The Bearded Screech-Owls at Huitepec were located in the

Northwest slope of the Reserve, which were also areas of higher humidity (Rami'rez-Marcial et al.

42 1996). These slopes with less direct sunlight can maintain more moisture and create desirable microclimatic conditions in the forest that owls might select (Hinam and Duncan 2002). No

Bearded Screech-Owls have been recorded in the drier eastern slopes of the reserve. Aspect direction is therefore a good predictor of Bearded Screech-Owl presence, at least at Huitepec.

This observation is supported by data from other owl species. North facing slopes are important for presence and roost sites for Northern Spotted Owls (Solis and Gutierrez 1990), Mexican

Spotted Owls (Young et al. 1998), Great Gray Owls and Barred Owls (Hinam and Duncan 2002).

Another habitat attribute related to Bearded Screech-Owl presence at Huitepec was the distance to intermittent water resource. Roosting and breeding sites close to water sources can be important for forest birds of prey because water sources attract an increase in diversity and abundance of prey items (Forsman et al. 1984, Bosakowski et al. 1987, Hargis et al. 1994).

At El Callejon, the high level of human activities has reduced the heterogeneity of the habitat compared to that of Huitepec. Zabel et al. (1995) identified factors that may allow owls to survive in young managed forests. Those forests could provide higher prey availability than mature forest. However more information on prey availability is needed for these kinds of forests.

The important attributes for Bearded Screech-Owl presence at El Callejon were similar to those at

Huitepec and included canopy cover, canopy height and distance to intermittent water (Table 3.4 and 3.6).

Home Ranges.- My data showed that the home range size for eight Bearded Screech-

Owl was highly variable (Table 3.5, Fig. 3.5). The home ranges described for other small owls have been also variable. For instance, home ranges varied from 8.5 to 24 ha (average14.5 ha;

McCallum 1994) for Flammulated Owls, from 8.8 to 107.5 ha for the Eastern Screech-Owl (Smith and Gilbert 1984), and from 3 to 58 ha for the Western Screech-Owl (Johnsgard 2002).

One hypotheses is predicts that small home ranges are associated with high food availability, while larger home ranges are associated with lower food availability (Schoener 1968,

Morris 1987, Carey et al. 1990). Carey et al. (1990) also proposed that old forests support more

43 prey abundance, thus home ranges should be smaller in this type of habitat. At Huitepec, invertebrates identified in the diet of the Bearded Screech-Owl (Coleoptera, Orthoptera, and

Aranae; Chapter 4), showed different distributions among vegetation types during a single dry season, and the moist oak forest tended to have higher abundance of invertebrates than the other vegetation types (Chavez-Zichinelli 2002). Moreover, at Huitepec the Bearded Screech-Owl was recorded only in moist oak forest and cloud forest. The prediction that home ranges would be smaller in mature forest was not supported by my Bearded Screech-Owl data, because Bearded

Screech-Owls in Huitepec had larger home ranges than those at El Callejon. On the other hand, home range size in El Callejon was more variable (from 4 to 30 ha) than in the Huitepec (Fig. 3.4) perhaps because the habitat was more patchy at El Callejon or the fragmentation of this area was also more variable. This might indicate that the food availability hypothesis over-rides the mature forest hypothesis. However, more studies on food availability between sites should be conducted.

Some studies have shown prey availability to be a better predictor for home range sizes than the amount of suitable habitat (Zabel et al. 1995, Glenn et al. 2004). However, many factors such as habitat availability, prey abundance, distribution, territoriality, sex, age, breeding season, and season interact to determine home range sizes of birds of prey (Newton 1979). Some of these factors could be more complex in areas of intensive and extensive changes in land use and where prey availability is changing rapidly (Bennet and Bloom 2005).

Huitepec constitutes one of the last remnants of mature forest protected in the Central

Highlands of Chiapas (Rami'rez-Marcial et al. 1998). Although the reserve is small (137 ha), it still contains 32% of the floristic richness of the region above 2000 m sea level (Gonzalez-Espinosa et al. 1997). Huitepec has been a protected area since 1987, before that local people cut branches for firewood, and they continue using the trails of the reserve for walking and transporting their sheep and dogs to other areas. At Huitepec, the Bearded Screech-Owl does not appear to depend exclusively on old growth forest. The habitat composition inside their home ranges was mainly moist oak forest at Huitepec and pine-oak at El Callejon. This owl species was

44 associated mainly with moist forested areas, and forest edges. Forest edges are an important component of habitat selected by Bearded Screech-Owl not only for foraging but also for roosting sites (see Chapter 4).

The main threat for species restricted to high elevations and narrow elevation ranges in a declining habitat is that they could face the limit of their warm range margin (spatial isolation) because of their inability to disperse to and inhabit new areas (Pounds et al. 1999, Wilson et al.

2005). The restricted distribution of this species in Chiapas could make it more vulnerable to extensive and intensive changes in land use occurring in the region.

Forest clearing, and subsequent land degradation, has become the major threat to forest ecosystems in the Highlands of Chiapas. Actually, the region in these highlands is a mosaic of fragmented forest stands having different stages of succession and isolation (Ochoa-Gaona and

Gonzalez-Espinosa 2000, Ochoa-Gaona et al. 2004). The highest resource demand from these forests is harvesting for wood, fuel wood, and charcoal, representing the most frequent disturbance factor in these forests (Ochoa-Gaona- Gonzalez-Espinosa 2000). The traditional forest use shows a general perturbation of moderate intensity but high frequency (Barron-Sevilla

2002). These activities are reducing the growth and regeneration of interior and canopy trees, and at the same time there is a local increase in distribution of pine forest, a loss of tree diversity and understory shrubs, and a decrease in soil fertility (Gonzalez-Espinosa et al. 1991, Ramirez-

Marcial et al. 2001). These changes may also alter microclimatic conditions by decreasing moisture in the understory and forest floor levels and increasing temperature variability (Ramfrez-

Marcial et al. 2001).

Some oak species from moist forest (e.g. Quercus laurina) can germinate in a wide variety of successional environments (e.g. pine dominated stands; Gonzalez-Espinosa et al.

1997, Camacho-Cruz et al. 2000). However, it will be crucial to limit harvesting large oak trees to allow greater recruitment of important oaks for conservation, not only for oak species per se but also for the fauna associated to oak species as the Bearded Screech-Owl.

45 In the highlands of Chiapas, the number of fragmented stands is increasing, but the size of these stands is decreasing (Ochoa-Gaona 2001). Canopy cover and understory tree species decrease as human disturbance increases (Ramirez-Marcial et al. 2001). The causal factors in levels of perturbation in forests of the Highlands of Chiapas vary with the land use history, environmental and socioeconomic attributes per site. In fact, each site has different patterns and intensities of forest disturbance, resulting in variation in forest structure and floristic composition.

Environmental factors such as slope, soil type, water resource availability and road access also affect the habitat structure and fauna in these forests (Ochoa-Gaona and Gonzalez-Espinosa

2000, Ochoa-Gaona 2001).

My study represents a first step in our understanding of habitat attributes associated with home ranges of the endemic and threatened Bearded Screech-Owl in the Central Highlands of

Chiapas. The habitat attributes associated to owl occurrence will be useful to make predictions of owl presence in other areas. Additional information on habitat selection and habitat use would aid in determining how selected habitat attributes influence occurrence patterns of the Bearded

Screech-Owl. Future research should estimate reproduction and survival rates and prey availability to determine if forest disturbance is reducing food availability. Thus, the conservation strategies for this threatened mountain owl should consider the local causal factors in levels of perturbation.

46 Table 3.1. Description of the environmental and physiographic habitat variables measured in plots with and without Bearded Screech-Owl detections in the Central Highlands of Chiapas, Mexico.

Environmental Variables ID Units Description Vegetation Types* VET Type of main vegetation. Forest: pine, oak, pine-oak, cloud forest, and managed oak. Strata Number STR Number of vertical strata in the vegetation Canopy Cover CAC % Mean of four measures per cardinal direction N, S, E, W taken with a densitometer Canopy Height CAH m Mean of five measures of tree canopy height using clinometers Shrub Height SHH m Mean of five shrub heights taken using clinometer Herb Height HEH cm Mean of five herbaceous heights taken using a rule

Diameter Breast High DBH cm Tree density included in each of five diameter categories: DBH1 (<5 cm), DBH2 (6 to 15 cm), DBH 3 (16 to 30 cm), DBH 4 (31 to 45 cm), and DBH 5 (> 45 cm) Tree Density TRD Trees/ha Density of all trees in the plot Undergrowth Cover UNC % Percent cover of undergrowth in the plot Litter Leaves LIL % Percent cover of leaf litter in he plot Herb Cover HEC % Percent cover of herbs in the plot Leaf Litter Depth LID cm Mean of five depths of leaf litter measured using a ruler Rocks ROC % Percent cover of rocks in the plot Epiphytes EPI % Percent cover of epiphytes in the plot Snags SNA Number of snags in the plot Logs LOG Number of logs in the plot (dead trees or portions of trees lavina on the forest flnnrt Physiographic Variables

Soil Type* SOT Type of soil Slope characteristic* Flat, gentle, undulating, and steep Slope SLO % Mean of five slope measures (angle between the horizontal and the plane of the ground surface) Elevation ELE m Elevation using an altimeter Table 3.1 (cont.). Description of the environmental and physiographic habitat variables measured in plots with and without Bearded Screech-Owl detections in the Central Highlands of Chiapas, Mexico.

Environmental Variables ID Units Description

Aspect* ASP Direction of the downhill slope (N, NE, E, SE, S, SW, W, NW) Erosion* ERO None, light, moderate, and intense Distance to water P DWP m Distance to permanent water resource Distance to water I DWI m Distance to nearest intermittent water

* Categorical variables (analyzed using chi-square).

oo Table 3.2. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl detections in the Central Highlands of Chiapas, Mexico.

Sites Variables Owl detected (N=56) No owl detected (N=56) Mean SE Mean SE P* Strata Number 2.55 0.5 2.30 0.65 0.05 Canopy Cover 95.49 0.74 77.07 2.29 0.001 Canopy Height 13.26 0.53 12.06 0.66 0.16 Shrub Height 2.11 0.22 1.84 0.12 0.36 Herb Height 22.03 2.42 16.48 1.16 0.15 DBH1 (<5 cm) 652.72 45.73 234.74 28.88 0.001 DBH2 (6 to 15 cm) 459.27 27.84 307.72 27.14 0.001 DBH3(16to 30 cm) 276.72 13.49 131.58 14.09 0.01 DBH4 (31 to 45 cm) 35.64 4.51 27.72 5.12 0.06 DBH5 (>45 cm) 16 2.95 14.74 3.30 0.39 Tree Density 1332.36 76.11 716.49 56.13 0.001 Undergrowth Cover 48.39 3.52 28.21 3.18 0.001 Litter Leaves 71.86 3.34 64.74 3.81 0.18 Herb Cover 28.2 3.34 35.28 3.82 0.18 Leaf Litter Depth 4.26 0.27 3.17 0.29 0.001 Rocks 6.29 2.21 18.04 3.26 0.001 Epiphytes 22.18 3.64 18.86 3.79 0.11 Snags 0.6 0.18 0.23 0.11 0.06 Logs 1.07 0.24 0.58 0.13 0.33 Slope 29.52 2.47 . 29.84 3.05 0.62 Elevation 2354.27 18.06 2343.28 16.71 0.66 Distance to permanent water 2.43 0.3 1.73 0.24 0.09 Distance to intermittent water 2.29 0.33 1.82 0.17 0.25 *P-values came from ANOVA.

49 Table 3.3. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected in the Central Highlands of Chiapas, Mexico.

Sites Variables Categories Owl detected No owl detected 0/ 0/ P /o /o Vegetation Types 0.001 Pine 16.07 7.14 Dry oak 0.00 44.64 Humid oak 26.78 5.36 Pine-oak 23.21 30.36 Cloud forest 25.00 8.93 Managed oak 8.93 3.57 Soil Type 0.12 Acrisol 12.50 16.07 Luvisol 50.00 39.28 Rendzina 37.50 44.64 Slope characteristic 0.44 Flat 16.07 25.00 Gentle 21.43 23.22 Steep 16.07 21.43 Undulanding 46.43 30.36 Aspect 0.06 North 33.93 19.64 Northeast 16.07 19.64 - Northwest 28.57 12.50 South 0.00 8.93 Southwest 1.78 10.71 East 10.71 19.65 West 8.93 8.93 Erosion 0.001 None 30.36 8.93 Light 62.50 50.00 Moderate 7.14 30.36 Intense 0.00 10.71 *P- values came from Chi-square tests.

50 Table 3.4. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl detections at Huitepec Biological Reserve, San Cristobal de Las Casas, Chiapas, Mexico.

Sites Variables Owl detected (N=18) No owl detected (N=12) Mean SE Mean SE P* Strata Number 2.71 0.13 2.94 0.06 0.12 Canopy Cover 97.98 0.58 92.95 0.62 0.001 Canopy Height 13.1 1.05 16.16 0.94 0.04 Shrub Height 1.78 0.2 2.19 0.15 0.1 Herb Height 18.11 1.52 15.18 1.21 0.14 DBH1 (<5 cm) 517.14 77.85 248.75 31.46 0.002 DBH2 (6 to 15 cm) 424.28 50.15 355 47.27 0.32 DBH3(16to 30 cm) 138.57 20.69 196.25 33.77 0.23 DBH4 (31 to 45 cm) 18.57 5.73 28.75 8.55 0.35 DBH5 (>45 cm) 18.57 6.09 25 8.06 0.54 Tree Density 1115.71 114.49 853.75 81.32 0.07 Undergrowth Cover 61.79 4.77 48.81 5.06 0.08 Litter Leaves 69.7 7.05 80.5 4.31 0.19 Herb Cover 30.3 7.05 19.5 4.31 0.19 Leaf Litter Depth 6.23 0.52 5.52 0.53 0.35 Rocks 4.07 2.45 6.56 2.31 0.46 Epiphytes 19.29 6.56 32.81 8.05 0.21 Snags 0.28 0.16 0.5 0.34 0.65 Logs 0.78 0.29 0.75 0.26 0.93 Slope 40.34 5.28 28.46 4.93 0.11 Elevation 2413.71 25.35 2387.94 28.26 0.51 Distance to permanent water 0.71 0.06 0.55 0.09 0.17 Distance to intermittent water 0.27 0.05 0.74 0.07 0.001 *P-values came from ANOVA.

51 Table 3.5. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected at Huitepec Biological Reserve, San Cristobal de las Casas, Chiapas, Mexico.

Sites Variables Categories Owl detected No owl detected % % P Vegetation Types 0.001 Dry oak 0.00 57.14 Humid oak 62.50 0.00 Cloud forest 25.00 28.57 Managed oak 12.50 14.29 Soil Type Luvisol Slope characteristic 0.33 Flat 7.14 18.75 Gentle 7.14 25.00 Steep 28.57 12.50 Undulanding 57.14 43.75 Aspect 0.09 North 50.00 12.50 Northeast 14.29 37.50 Northwest 21.43 12.50 Southeast 0.00 12.50 East 7.14 25.00 West 7.14 0.00 Erosion 0.35 None 28.57 18.75 Light 71.42 68.75 Moderate 0.00 12.50

52 Table 3.6. Mean values of vegetation and physiographic variables at survey points with and without Bearded Screech-Owl detections at El Callejon, San Cristobal de las Casas, Chiapas, Mexico.

Sites Variables Owl detected (N=10) No owl detected (N=10) Mean SE Mean SE P* Strata Number 2.3 0.15 2.3 0.21 Canopy Cover 98.61 0.33 76.41 3.41 0.001 Canopy Height 15.04 1.08 9.37 0.86 0.001 Shrub Height 2.31 0.17 1.43 0.06 0.001 Herb Height 11.83 0.91 16.78 2.48 0.16 DBH1 (<5 cm) 248 28.15 274 42.06 0.61 DBH2 (6 to 15 cm) 502 52.36 302 47.46 0.01 DBH3(16to 30 cm) 168 29.84 128 21.12 0.28 DBH4 (31 to 45 cm) 34 10.34 28 9.04 0.67 DBH5 (>45 cm) 18 6.28 10 4.47 0.31 Tree Density 968 78.89 742 89.61 0.07 Undergrowth Cover 29.58 5.4 23.48 7.09 0.5 Litter Leaves 89.78 3.56 59.76 6.89 0.001 Herb Cover 10.22 3.56 40.24 6.86 0.001 Leaf Litter Depth 3.15 0.24 2.85 0.32 0.47 Rocks 0.5 0.5 17.3 5.82 0.01 Epiphytes 3.5 1.3 19 6.69 0.13 Snags 0.09 0.2 0.13 0.14 Logs 0.12 0.5 0.16 0.01 Slope 27.57 6.03 31.02 10.69 0.78 Elevation 2211.3 15.71 2355.7 14.75 0.001 Distance to permanent water 3.95 0.05 2.69 0.71 0.13 Distance to intermittent water 5.37 0.08 2.93 0.35 0.002 *P-values came from ANOVA

53 Table 3.7. Percent of sites under different vegetation and physiographic categories where Bearded Screech-Owls were detected at El Callejon, San Cristobal de las Casas, Chiapas, Mexico.

Sites Variables Categories Owl detected No owl detected /o /o P Vegetation Types 0.26 Pine-oak 72.73 100.00 Pine 27.27 0.00 Soil Type 0.3 Luvisol 0.00 10.00 Rendzina 100.00 90.00 Slope characteristic 0.6 Flat 20.00 40.00 Gentle 20.00 10.00 Steep 20.00 30.00 Undulanding 40.00 20.00 Aspect 0.1 North 27.27 11.11 Northeast 54.54 0.00 South 0.00 33.33 Southweast 9.10 22.22 East 9.10 11.11 West 0.00 22.22 Erosion 0.58 Light 80.00 70.00 Moderate 20.00 20.00 Intense 0.00 10.00

54 Table 3.8. Home-range size of eight adult (AHY) Bearded Screech-Owls in the Central Highlands of Chiapas, Mexico, based on 95% fixed-kernel estimates.

Study Area Sex Locations Tracking Period Home range size (n) (ha) Huitepec Biological Reserve male 20 5/Jul/2002-4/Oct/2002 28.59 Huitepec Biological Reserve male 25 27/Jul/2002-8/Nov/2002 32.56 Huitepec Biological Reserve female 28 2/Feb/2004-1 /Apr/2004 22.91 Huitepec Biological Reserve male 38 2/Feb/2004-19/Apr/2004 36.85 El Callejon female 43 14/Feb/2004-24/Apr/2004 8.51 El Callejon male 28 14/Apr/2004-26/Jun/2004 4.13 El Callejon male 12 1 /May/2004-25/May/2004 15.09 El Callejon female 10 7/Jul/2004-1/Aug/2004 30.41

55 Figure 3.1. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Screech-Owl detections in the Central Highlands of Chiapas. Four habitat attributes included in the model were: Canopy cover, diameter at breast height < 5 cm (DBH1), canopy height, and leaf litter depth. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours.

56 Figure 3.2. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Screech-Owl in the Huitepec Biological Reserve, San Cristobal de las Casas. Five habitat attributes included in the model were: Canopy cover, diameter at breast height < 5 cm (DBH1), diameter at breast height 16 to 30 cm (DBH3), slope, and distance to permanent water. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours.

57 Figure 3.3. Canonical Analysis of Discriminance (CAD) for sites with (1) and without (0) Bearded Bearded Screech-Owl in the El Callejon, San Cristobal de las Casas, Chiapas. Four habitat attributes included in the model were: Canopy cover, shrub height, distance to permanent water, and epiphytes. Canonical axes represent standardized values of transformed variables. Internal circles represent to 95% confident limits for the group mean, and the external circles contain 50% of the normal contours

58 40

30

CO X 20-^

1(H

El Callejon Huitepec

Location

Figure 3.4. Box-plots of home range size (ha) of Bearded Screech-owls at El Callejon and Huitepec sites, Central Highlands of Chiapas, Mexico. Boxes represent the 10th and 90th percentiles, the line within each box represents the median, and bars represent 5th and 95"

percentiles. F1f6 = 5.88, P= 0.051.

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63 Ramfrez-Marcial, N., S. Ochoa-Gaona, M. Gonzalez-Espinosa, and P. F. Quintana-Ascencio. 1998. Analisis floristico y sucesional en la Estacion Biologica Cerro Huitepec, Chiapas, Mexico. Acta Botanica Mexicana 44: 59-85. Ramirez-Marcial, N., M. Gonzalez-Espinosa, and G. Williams-Linera. 2001. Anthropogenic disturbance and tree diversity in montane rain forest in Chiapas, Mexico. Forest Ecology and Management 154: 311 -326. Rodriguez-Estrella, R. and A. Pelaez. 2003. The western screech owl and habitat alteration in Baja California: a gradient from urban and rural landscapes to natural habitat. Canadian Journal of Zoology 81: 916-922. Rzedowski, J. 1978. Vegetacion de Mexico. Limusa, Mexico, D. F. 432p. Sail, J., L. Creighton, and A. Lehman. 2005. JMP Start Statistics. SAS Institute Inc. 3th Ed. SAS Institute Inc. Thompson Learning, Belmont, California, USA. Samuel, M. D. and M. R. Fuller. 1994. Wildlife Radiotelemetry Pp. 370-418. In T. A. Bookhout (Ed.) Research and Management Techniques for Wildlife and Habitats. 5th Ed. The Wildlife Society, Bethesda, MD. 740p Schoener, T. W. 1968. Size of feeding territories among birds. Ecology 49: 123-141. Seaman, D. E. and R. A. Powell. 1991. Kernel Home Range Estimation Program (Kernel HR), Version 4.27, 1997. North Carolina State University. NC, USA. Seaman, D. E., B. Griffith and R. A. Powell. 1998. KERNELHR: a program for estimating animal home ranges. Wildlife Society Bulletin 26: 95-100. Smith, D. G. and R. Gilbert. 1984. Eastern Screech-Owl home range and use of suburban habitats in southern Connecticut. Journal of Field Ornithologist 55: 322-329. Solis, D. M. Jr. and R. J. Gutierrez. 1990. Summer habitat ecology of Northern Spotted Owls in Northwestern California. Condor 92: 739-748. Statterfield, A. J., M. J. Crosboy, A. J. Long and D. C. Wege. 1998. Endemic bird areas of the world. Priorities for Biodiversity Conservation. Birdlife Conservation Serie 7. Bird Life International, Cambridge, UK. Wagner, P. L. 1962. Natural and artificial zonation in a vegetation cover: Chiapas, Mexico. Geographical Review 52: 252-274. Ward, J. P. Jr., R. J. Gutierrez, and B. R. Noon. 1998. Habitat selection by Northern Spotted Owls: The consequences of prey selection and distribution. Condor 100: 79-92. Wilson, R. J., D. Gutierrez, J. Gutierrez, D. Martinez, R. Agudo, and V. J. M. Monserrat. 2005. Changes to the elevational limits and extent of species ranges associated with climate change. Ecology Letters 8: 1138-1146.

64 Winton, B. R. and D. M. Leslie, Jr. 2004. Density and habitat associations of Barred Owls at the edge of their range in Okalhoma. Southestern Naturalist 3: 475-482. Worton, B. J. 1989. Kernel Methods for estimating the utilization distribution in home-range studies. Ecology 70: 164-168. Young, K. E., R. Valdez, P. J. Zwank and W. R. Gould. 1998. Density and roost site characteristic of Spotted Owls in the Sierra Madre Occidental, Chihuahua, Mexico. Condor 100: 732- 736. Zabel, C. J., K. McKelvey, and J. P. Ward Jr. 1995. Influence of primary prey on home-range size and habitat-use pattern of northern spotted owls {Strix occidentalis caurina). Canadian Journal of Zoology 73: 433-439. Zar, J.H. 1999. Biostatistical Analysis. Prentice Hall, New Jersey, N.J., USA. Zwank, P. J. 1995. Density estimates and habitat use by Flammulated Owls in Southern New Mexico. Pp. 475-478. In J. A. Bissonette and P. R. Krausman (Eds.). Integrating people and wildlife for a sustainable future. The Wildlife Society, Bethesda, MD.

65 CHAPTER 4:

NATURAL HISTORY OF THE BEARDED SCREECH-OWL IN CHIAPAS1

INTRODUCTION

The Bearded Screech-Owl (Megascops barbarus) is an endemic species of the northern

Neotropics, restricted to tropical montane forests in elevations from 1800 to 2500 m in Chiapas

(Southern Mexico) and Guatemala. Limited information about its natural history has been reported. Even its eggs and nest have not been described (Howell and Webb 1995, Holt et al.

1999, Konig et al. 1999). Based on its restricted distribution and the lack of ecological information this species has been listed as threatened in the Mexican Red List and near threatened globally

(DOF 2002, Bird Life International 2004). Furthermore, tropical montane forests are considered among the world's most threatened ecosystems (Myers et al. 2000, Kappelle and Brown 2001).

These forest habitats in the Central highlands of Chiapas have been fragmented and reduced at an annual rate of £2.7 percent (Ochoa-Gaona and Gonzalez-Espinosa 2000, Cayuela et al.

2006). Logging for firewood and charcoal, agricultural expansion, and urbanization have reduced the forest cover and increased the proportion of edges and disturbed forests (Ramirez-Marcial et al. 2001). The effects of habitat disturbance on wildlife species in the Central Highlands of

Chiapas are poorly known. Changes in land-use patterns in the region may affect the availability of resources used by birds from old-growth forests and seriously threatening birds persistence

(Gonzalez-Espinosa et al. 1995).

Knowing the natural history characteristics and the strategies that a species adopts may enable us to understand how it responds to environmental changes. Most of the birds inhabiting tropical montane forests are characterized by 'slow' life history traits (i.e., high survival rates combined with low reproductive rates; Bennett and Owen 2002), making them sensitive to environmental changes and vulnerable to extinction (Watson and Peterson 1999). Moreover,

1 Paper submitted to The Journal of Raptor Research. 66 some predators (e.g., many owl species) are highly sensitive to habitat fragmentation (Shoener

1989). Here I describe the morphological characteristics, nest site, home ranges, roost-sites and diet of the Bearded Screech-Owl in the Highlands of Chiapas, Mexico.

STUDY AREA AND METHODS

Most of the information for this study was obtained at the Huitepec Biological Reserve

(16° 44' 38"N and 92° 40'15"W; elevation ranges from 2 230 to 2 710 m above sea-level) in the

Central Highlands of Chiapas, Mexico. The reserve (137 ha) is located approximately 3.5 km W of San Cristobal de las Casas and has very steep slopes (i.e., 40 to 60 degrees). The mean annual temperature ranges from 13° to 15°C, and the mean annual precipitation ranges from

1100 to 1200 mm (Garcia 1988, Ramirez-Marcial et al. 1998). The rainy season is from May to

October, and the dry season from November to April. Vegetation is mainly oak forest including eight Quercus (Fagaceae) species as well as Arbutus xalapensis (Ericaceae), Alnus acuminata

(Betulaceae), Oreopanax xalapensis (Araliaceae), Rapanea juergensenii (Myrsinaceae), and

Styrax argenteus (Styracaceae). There are scattered communities of pine-oak forest at the west of the reserve, and elements of cloud forest occur in the higher areas which include Quercus laurina, Q. crassifolia, Clethra macrophylla (Clethraceae), Cleyera theaeoides (Theaceae), and

Persea americana (Lauraceae). A detailed description of the vegetation for this area can be found in Ramirez-Marcial et al. (1998).

Fourteen Bearded Screech-Owls were captured within their respective territories between

July to November 2002, February to April 2003, and January to August 2004 using broadcasts of pre-recorded conspecific calls and two standard mist-nets (2.5 m high x 12.0 m length, 36 mm mesh), set up for two to four hours each night (Fuller and Mosher 1987). Each owl captured was measured (wing chord, tail, tarsus, culmen, and keel); the keel length was measured from the base of the sternum to the superior base close to the furcula. I also weighed and examined each

individual for moult pattern and subcutaneous fat. Owls were banded with a numbered aluminium

67 leg band and sexed by voice (female has higher-pitched vocalization than males; Konig et al.

1999) or by the presence of a brood patch (found in females only).

I obtained morphometric measurements from 15 skins (12 from Chiapas and 3 from

Guatemala) from 6 museums (The University of Kansas Natural History Museum [KUNHM] female 35072; The Western Foundation of Vertebrate Zoology [WFVZ] male 10253; Coleccion

Zoologica Regional de Aves- Instituto de Historia Natural y Ecologia de Chiapas [CZRAV], 3 females 5158, 5513, 6542, 4 males 202, 203, 205, 5117, unknown 204; The American Museum of Natural History [AMNH] female 808831 and unknown 71493; The National Museum of Natural

History [USNM] female 150916 and unknown 42776; The Royal Ontario Museum [ROM] female

118412).

I analyzed the morphometric data from captured owls and museum skins separately using paired Mests to evaluate differences in morphology between sexes. Prior to statistical analysis, data residuals were checked for statistical normality with Shapiro-Wilks (W) test and equal variance with Bartlett's test (Gotelli and Ellison 2004). Statistical test differences were considered significant at P-value < 0.05.

From 2002-04 I tracked 8 owls equipped with backpack-style radio transmitters (Holohil

Systems Ltd. Ontario, Canada) to determine home range size, and found one nest in 2001 also described here. The radio transmitter and harness weighed 1.95g. Transmitter battery life was approximately 16 weeks. An H-antenna with flexible elements and portable receivers (Telonics

Inc. Mesa, AZ, USA) were used to receive radio signals. Home range sizes of owls were determined using the Fixed Kernel Home Range Method 95% (Worton 1989) with the KernelHR

Program (Seaman and Powell 1991). A reflectance tag was attached to the antenna to facilitate the location owls at night and observed foraging. Because tags detach from antennas after a few weeks, visual sampling was limited 8 h in total. When day roosts of radio-marked owls were found site characteristics, including tree height, diameter at breast height (DBH), and roost height were recorded. When was possible r adio transmitter were removed after the study.

68 Because Bearded Screech-Owls do not regularly produce pellets of non-digested prey material, I examined their feces preserved in alcohol to study their diet (Lee and Severinghaus

2004). Prey items were identified using a reference collection of insects captured at night. The proportional biomass of each prey in the diet was estimated by multiplying the number of individuals times the mean body weight of the species (Rosenberg and Cooper 1990).

RESULTS

Overall, data were collected from 39 Bearded Screech-Owls; 14 owls captured for this study, 10 live owls from a concurrent study at the Huitepec Biological Reserve (Rangel-Salazar and Enriquez 2004), and 15 museum skins.

Morphology and Moult.- Among live owls, females were heavier than males (f = - 3.35, P

< 0.01) and had longer tails than males (f = - 5.14, P< 0.01; Table 4.1), but wing chord, tarsus, culmen, keel and middle toe lengths were similar between sexes (Table 4.1). Morphological data from museum skins also varied between sexes but not significantly (P < 0.05).

The plumage colour morphs for the captured Bearded Screech-Owls were greyish-brown and red (rufous). Five of the 8 females and one of 6 males at Huitepec were red morph (42.8%).

Of three owl specimens from Guatemala, one female was red and two owls of unknown sex were of intermediate colour (mix of greyish-brown and red; D. James pers. comm.).

Bearded Screech-Owls moulted in the rainy season, from July to October (n = 12), with

July being the peak of moulting (i.e. heaviest levels of moult per individual in July; n= 8; Fig. 4.1).

Most of the primary remiges were moulted (two at a time) in July in ascending order and usually simultaneously on both wings. Secondary remiges were moulted at the same time and in the same manner as the primaries. Similar to some other owl species, tail moults were partial

(gradual or irregular) or complete ("simultaneous"; Forsman 1981). Simultaneous tail moult was recorded in two individuals captured with no rectrices and in both cases the birds were also

69 heavily moulting contour feathers. Two other individuals had partial rectrices moult: one moulting r1 and r2 right and the other moulting r3 and r4 on both sides.

Nesting -1 found one nest on 26 June 2001 in a natural cavity of a large living oak tree

(Quercus laurina; 16°45'50"N; 92°40'96"W), at 2 250 m elevation. The oak tree had a DBH of 74 cm and a height of 22 m. The nest cavity was 2.45 m above ground, was 45 cm long, 20 cm wide and 5 cm deep, and faced north (this side having higher humidity). Inside the cavity, an adult red morph female was brooding a single grey-beaked nestling (Fig. 4.2), approximately three weeks old. Inside the nest, there was no apparent nesting material, only a few mosses and insect prey remains. Pellets or feces were not found inside or near the nest. This cavity was not used subsequently through 2004 and no other nest was found for the rest of the study period.

The type of vegetation in the nest area was moist oak forest, and the dominant tree species were Quercus rugosa, Q. crassifolia, Q. laurina, Oreopanax xalapensis, Viburnum jucundum (Caprifoliaceae), Arbutus jalapensis, and Cornus excelsa (Cornaceae). The main shrubs were Eupatorium mairetianum (Asteraceae), Rapanea juergensenii, and Rhamnus mcvaughii (Rhamnaceae). Nest-site habitat (inside a 0.05 ha plot) was characterised by a mean tree canopy height of 16.14 m, and a maximum tree canopy height of 22.05 m, three old trees were present with DBH over 31 cm. Most of the trees around the nest tree varied from 6 to 15 cm

DBH and the tree density was 640 trees/ha. Under story cover was 3 percent, the slope in the area was undulating (36°), and the distance to a temporal stream was 200 m. The fact that this active nest was found in June and two females with brood patch captured in April during this study (Fig. 4.1), suggests that the nesting period for Bearded Screech-Owl starts in March or April with laying and incubation, and brooding and fledging in May through July.

Natural History.- I established a longevity record of 4 yrs 2 months, for a female first captured as an adult (at least 1 yr old) in July 1998 in the moist oak forest at the Huitepec

Biological Reserve. This female was recaptured in May 1999 and August 2001. The distance between initial capture and recapture locations was approximately 1 Km. A second female, also

70 an adult, was first captured in July 1997 as an adult, was recaptured in October 1997, April 1998, and January 1999, at the same site in the cloud forest. As of last capture, she was at least 2 yrs 8 months old.

The mean home range size of 8 radio-tracked owls was 22.38 ± 4.21 ha. The mean home range size for 3 females was 20.61 ± 6.42 ha and the mean for 5 males was 23.44 ± 6.05 ha.

I found four daytime roost sites within the Huitepec Biological Reserve. Two were in trees of Clethra macrophylla, and two were in Pinus ayacahuite (Pinaceae). The roost characteristics of the two C. macrophylla were: roost height = 2.52 m and 3 m, tree height = 3.3 m and 4.5 m, and

DBH = 10.2 cm and 24 cm, respectively. The roost characteristics of the two P. ayacahuite were: roost height = 4.34 m and 3.70 m, tree height = 11.3 m and 9.2 m, and DBH - 47.2 cm and 45cm, respectively. The foliage density in Bearded Screech-Owl roost-sites was important for concealment, and perhaps also for protection against the wind. All four roosting trees were located along forest edges with bushes, approximately 18 ± 5 m from the open area.

Night observations of two radio-marked Bearded Screech-Owls indicated that they hunted in the understory using a sit-and-wait strategy. When prey was located (either by sight or sound) from a perch, the owl flew to the ground gleaned prey from nearby substrates with its talons or beak. Prey (Coleoptera and Orthoptera insects) was then consumed at the site of capture or was brought back to the perch before consumption. Foraging substrates used were woody surfaces (such as tree trunks), leaf litter, and the ground. After consuming prey at night, owls usually took a rest for 10-15 min on a perch. No pellets were found under perches.

Prey items found in 16 fecal samples all consisted of invertebrates (Table 4.2). The most common food items identified were Coleoptera; Melonontidae (72.3 %) and Carabidae (7.7 %).

Orthoptera (9.2 %), Lepidoptera (3.1%) and Arachnida (1.5%) were also found. Melonontidae and Gryllacrididae contributed most to the biomass. Food remains identified in the nest were cockroaches, crickets, moths of the family Noctuidae, and beetles from the genus Phyllophaga

71 sp. (Melonontidae). Additionally, the stomach contents from two females included caterpillars, beetles, a wingless roach, spiders, and scorpions (KUNHM 35072 and ROM 118412).

DISCUSSION

The Bearded Screech-Owl has been listed as near threatened globally (Bird Life

International 2004) and as threatened in the Mexican Red List (DOF 2002) based on its restricted distribution and the lack of ecological information. After three field seasons (2002 - 2004) of intensive searching I observed few individuals, captured just 14 birds, recorded 40 calling birds

(see Chapter 2) in an area of 4 000 km2 and found just one nest. Thus, my results support that the species is quite rare in some areas but uncommon in others (Chapter 2). It t could be especially susceptible to further loss of habitat or reduced nest sites availability.

Morphology and Moult - Prior to this study, for this species there had been only morphometric information available from museum specimens. Similar to some other Megascops

(Fitzpatrick and O'Neill 1986, Gehlbach 1995, Gehlbach and Gehlbach 2000, Cannings and

Angell 2001, Gehlbach 2003), Bearded Screech-Owl females are larger than males, showing reversed sexual dimorphism in body mass and tail, but not in wing chord, tarsus, and culmen.

The polymorphism in plumage colour has been described in some owl species (Marshall

1967, Galeotti and Rubolini 2004). Most of the Bearded Screech-Owl females captured were red

(rufous), and most of the males were greyish-brown. Some authors state that red morphs are more frequent in cloudy, moist, and shaded forests (Gehlbach 1995), and the different colour morphs may utilize different ecological niches (Galeotti and Rubolini 2004). The Bearded

Screech-Owls captured in this study did not support a relationshipc between plumage colour and specific habitats. Further data collection will be needed to examine colour morph variation in the

Bearded Screech-Owl.

Bearded Screech-Owls in this study started moulting at the end of the breeding season

(July - October). Moulting after breeding has also been reported for other screech-owl species in

72 North America (McCallum 1994, Cannings and Angell 2001, Gehlbach and Gehlbach 2000).

Also, the moult pattern of primary feathers and tail in the Bearded Screech-Owl appears to be similar to the moulting pattern reported for the Spotted Owl (Strix occidentalis; Forsman 1981).

/Vesf/ngt.-Understanding a threatened species' population biology and ecology is necessary to establish strategies to preserve it (Derrickson et al. 1998). One important factor affecting the survival of the species is reproduction, including nest-site selection. The first nest described herein for the Bearded Screech-Owl was found in a natural cavity in an old oak

(Quercus). As in other screech-owls, the Bearded Screech-Owl is likely an obligate secondary cavity nester which depends mainly on finding a suitable cavity for nesting. Quercus trees in the highlands of Chiapas have been selectively logged mainly for use as fuel wood and charcoal.

This has affected not only the canopy structure and the flora composition, but has also restricted conditions for many understory shrubs and trees, and thus, habitat for wildlife (Gonzalez-

Espinosa et al. 1995). Overall forest habitat conditions for this owl are declining at a significant rate (e.g. s 2.7% per year), with fragmentation and alteration a significant landscape issue.

Unlike some other screech-owls whose nest sanitation is minimal (McCallum 1994,

Gehlbach 1995, Gehlbach and Gehlbach 2000), the Bearded Screech-Owl maintains a very clean nest and I found only prey remains within the nest but no feces or pellets. The only other screech- owl species that exhibits a similar behaviour is the Western Screech-Owl (M. kennicottii), whose females keep the nest cavity clean during incubating and brooding, and often fly to a close perch for defecation and to drop pellets (Cannings and Angell 2001).

Two life-history processes that require high-energy investments in birds are breeding and moulting. Two females captured with brood patches in April, and the active nest found in June, suggests that the breeding season for Bearded Screech-Owl starts in the last part of the dry season and the early part of the rainy season. Similar to many tropical owl species (Holt et al.

1999, Currie et al. 2004), the Bearded Screech-Owl's breeding season likely starts in March or

April (egg laying), with the incubation and nestling period from March to May, and the fledging

73 period from June to July (Severinghaus 1992, Enriquez et al. 1997, Gehlbach and Gehlbach

2000, Currie et al. 2004). During the fledging period (rainy season), food availability may be abundant for fledgling development (del Hoyo et al. 1999). Gehlbach and Gehlbach (2000) reported that the Whiskered Screech-Owl (M. trichopsis), a species sympatric with the Bearded

Screech-Owl in the central highlands of Chiapas, started laying eggs around March 14, with an incubation period of 24 to 30 days (mean = 26.2).

Fat storage is known to be important in migratory birds (Benson and Winker 2005), but has rarely been studied in non-migratory bird species. Based on my observation, the Bearded

Screech-Owl is a local resident species. While its subcutaneous fat was evident throughout the year, it was more evident during the dry season. Fat storage in the Bearded Screech-Owl appears to respond to energetic needs (insulation and energy reserves; Welty 1982) because it coincides with the dry and cold season, with months of low temperatures (0-5 °C) at the Huitepec

Biological Reserve.

Natural History.- In general, Megascops owls are long-lived species. For example, the

Eastern Screech-Owl (M. asio) and Western Screech-Owl have been reported to live up to 13 or

14 years (Gehlbach 1995, Cannings and Angell 2001). At least one Bearded Screech-Owls that I encountered was estimated to be more than four years old. More long-term band return data will be needed to determine the life span of the Bearded Screech-Owl.

The home range sizes for this species are consistent with general expectations of this small, tropical forest insectivore predator (McCallum 1994, Johnsgard 2002). Additional radio- telemetry efforts are needed to acquire year-round data on mated pairs of owls; this data will likely offer new insights on the total habitat required by the owls, as well as more specific data necessary for the development of scientifically-sound conservation strategies for this owl (See

Chapter 3).

Habitat features and food availability influence foraging strategies. Similar to most forest owls, Bearded Screech-Owls hunt from perches and use the 'sit-and-wait' strategy (Norberg

74 1987). The diet composition consisted mainly of arthropods, dominated by Coleoptera of the

Melonontidae family. This is the most abundant beetle in the oak forest at the Huitepec Biological

Reserve (Moron-Rios and Huerta-Lwanga 2006). Beetles from Phyllophaga spp have also been recorded as food for the Whiskered Screech-Owl (Gehlbach and Gehlbach 2000), which may compete for food with the Bearded Screech-Owl.

My research demonstrated that a long term monitoring program to obtain further information on spatial and temporal variation on life-history parameters, breeding ecology, demography, and habitat use patterns of the Bearded Screech-Owl is necessary. There is a need to associate measures of population performance and habitat, but also a need to identify factors constraining the distribution and abundance of species (Morrison 2001). This work will be essential in order to develop a conservation strategy for this owl species, which is faces widespread habitat degradation.

75 Table 4.1. Morphological characteristics of captured individuals of the Bearded Screech-Owl in Chiapas. Data shown are mean (±SD; sample

size) and range. /-tests compared females and males. Bold font represents a significant difference.

Category Sex /-statistic P value Female (n=8) Male (n=5) Unknown Body mass (g) 71.86(1.72)62.5-79 62.96 (1.89) 58-69.5 67.18 (0.88; 8) 62.5-71.1 -3.35 0.006

Wing chord (mm) 137.1 (1.03) 131-140 134.9(1.46) 129-138 133.12 (0.95; 8) 130-138 r1.30 0.217

Tall (mm) 63.56 (0.17)63.3- 68.5 61.60(0.40)61-63 57.20 (4.44; 5) 40-64 -5.14 0.002

Tarsus (mm) 29.91 (0.62)25.9-31.5 30 (0.52) 28-31 29.88 (0.87; 7) 26-32.9 CD 0.10 0.924

Culmen (mm) 14.36 (0.76) 11.8-17.7 15.15 (0.23) 14.5-15.9 15.83 (0.67; 6) 13.4-17.5 0.79 0.445

Keel (mm) 22.23 (0.51)20-24.6 22.06 (0.85) 20-24.9 20.60 (1.17; 5) 17.7- 24.9 0.18 0.858

3 Middle toe" (mm) 16.15(1.15) 15-17.3 b 13.77 (0.64) 12.8-15 Na 1.99 0.14

Middle toe measured from distal end of tarsus to base of nail. (a n = 2,b n = 3 ). Na = not available. Table 4.2. Invertebrate prey remains found in 16 feces from 14 Bearded Screech-Owls captured in Chiapas, Mexico.

Prey Frequency Biomass

remains Family Weight (g) (%) (%) Arachnids

Arachnidae 0.5 1.53 1.32

Insects

Coleoptera Crysomelidae 0.5 3.08 2.63

Carabidae 0.5 7.69 6.58

Melonontidae 0.5 72.31 61.84

Orthoptera Gryllacrididae 1.5 4.62 11.84

Blattidae 1.0 4.62 7.89

Lepidoptera Noctuidae 1.0 3.07 5.26

Unidentified 0.5 3.08 2.63

Total 100 100

77 Breeding

Body moult

Primary moult

Secondary moult

Tail moult

1 I Visible fat

—i 1 1 1 \ 1 1 1 Jan -~i Feb 'Ma—r r~Apr May Jun Jul Aug Sep Oct Nov Dec

Figure 4.1. Annual cycle of breeding, moulting, and fat accumulation for the Bearded Screech- Owl in the Highlands of Chiapas, Mexico.

78 Figure 4.2. Nest of the Bearded Screech-Owl with red-phase female and gray phase nestling in a natural oak cavity in Huitepec Biological Reserve, Chiapas, Mexico. June, 2001. (Photo by Jose Luis Rangel-Salazar).

79 REFERENCES

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81 Marshall, J. T. Jr. 1967. Parallel variation in North and Middle America screech-owls. Monographs of the Western Foundation of Vertebrate Zoology 1: 72. McCallum, D.A. 1994. Flammulated Owl (Otus flammeolus). In A. Poole and F. Gill (Eds.) The Birds of North America, no. 93. Philadelphia, PA: Academy of Natural Sciences; Washington, DC. American Ornithologists' Union. Moron-Rios, A. and E. Huerta-Lwanga. 2006. Soil macrofauna of two successional evergreen cloud forest stages from the Cerro Huitepec Nature Reserve, San Cristobal de las Casas, Chiapas, Mexico. Interciencia 31: 611-615. Morrison, M. L. 2001. A proposed research emphasis to overcome the limits of wildlife-habitat relationship studies. Journal of Wildlife Management 65: 613-623. Myers, N., R. Mittermeier, C. Mittermeier, G. da Fonseca, and J. Kent. 2000. Biodiversity hot spots for conservation priorities. Nature 403:853-858. Norberg, A.R. 1987. Evolution, structure, and ecology of northern forest owls. Pp. 9-43. In R. W. Nero, R.J. Clark, R. J. Knapton, and R. H. Hamre. (Eds.) Biology and Conservation of Northern Forest Owls. Fort Collins, CO. USDA Forest Service. Ochoa-Gaona, S. and M. Gonzalez-Espinosa. 2000. Land use patterns and deforestation in the highlands of Chiapas, Mexico. Applied Geography 20:17-42. Ramirez-Marcial, N., S. Ochoa-Gaona, M. Gonzalez-Espinosa, and P. F. Quintana-Ascencio. 1998. Analisis florfstico y sucesional en la Estacion Biologica Cerro Huitepec, Chiapas, Mexico. Acta Botanica Mexicana 44: 59-85. Ramirez-Marcial, N., M. Gonzalez-Espinosa, and G. Williams-Linera. 2001. Anthropogenic disturbance and tree diversity in montane rain forests in Chiapas, Mexico. Forest Ecology and Management 154: 311 -326. Rangel-Salazar, J.L. and P.L. Enriquez. 2004. Ecologia para la conservacion de comunidades y poblaciones de aves en la Reserva Biologica Cerro Huitepec, Chiapas. El Colegio de la Frontera Sur, Chiapas, Mexico. Technical Report. 17p. Rosenberg, K.V. and R. J. Cooper.1990. Approaches to avian diet analysis. Pp. 80-90. In M.L. Morrison, C. J. Ralph, J. Verner, and J. R. Jehl Jr. (Eds.). Studies in Avian Biology 13. Cooper Ornithological Society. Seaman, D. E. and R. A. Powell. 1991. Kernel Home Range Estimation Program (Kernel HR), Version 4.27, 1997. North Carolina State University. NC, USA. Severinghaus, L.L. 1992. Monitoring the population of the endangered Lanyu Scops Owl (Otus elegans botolensis). Pp. 790-802. In McCullough, D.R. and R. H. Barrett (Eds.) Wildlife 2001: Populations. London England. Elsevier Science.

82 Shoener, T.W. 1989. Food webs from the small to the large. Ecology 70: 1559-1589. Watson, D. M. and A. T. Peterson. 1999. Determinants of diversity in a naturally fragmented landscape: humid montane forest avifaunas of Mesoamerica. Ecography 22: 582-589. Welty, J.C. 1982. The Life of Birds. 3th ed. New York, NY. Ed. Saunders College Publ. Worton, B. J. 1989. Kernel Methods for estimating the utilization distribution in home-range studies. Ecology 70: 164-168.

83 CHAPTER 5:

DIET AND TROPHIC ASSESSMENT OF THE BEARDED SCREECH-OWL USING 613C AND 615N

STABLE-ISOTOPES

INTRODUCTION

Diet plays a significant role in the health and viability of organisms while their trophic relationships define their ecological functions. Since the abundance of food types varies greatly in space and time (Recher 1990), a large number of animal species show a wide intra-specific and temporal variation in diet patterns (Dalerum and Angerbjorn 2005). Recent studies have included stable isotope analysis as an alternative method to determine the habitats within which an organism feeds (i.e. food origin; Mizutani et al. 1990, Hobson and Sealy 1991, Hobson and Clark

1992a), to evaluate spatial-temporal variation in diets, and to establish trophic position in birds and mammals (Hobson and Montevecchi 1991, Urton and Hobson 2005).

Stable isotope analysis will not reflect the bulk diet composition but will allow quantification of the diet origin of assimilated nutrients in animal tissues (Kelly 2000). Based on

C3 and C4 plants having distinct carbon-isotope signatures (Hobson and Sealy 1991), the stable-

carbon isotope analysis can distinguish C3 plants which are associated with moist habitats and

13 have low 5 C values, from C4 plants and CAM (Crassulacean Acid Metabolism) that are associated with drier habitats and exhibiting higher 513C values (Marra et al. 1998, Kelly 2000).

The stable- nitrogen isotope analysis determines the trophic level, since there is an enrichment of

515N at each trophic level (i.e. more positive nitrogen values will be in a higher level of food chain than animals with lower nitrogen; Gannes et al. 1997).

Studying stable isotopes in metabolically non-active tissues such as feathers (Duxbury and Holroyd 1997) will only reflect the dietary habits during the feather- growth period (Mizutani et al. 1990). Empirical studies have shown that birds can feed in different environments during

moulting and the synthesized protein from feathers reflects variation in isotopic values (Hobson

84 and Clark 1992a). Nevertheless, it is possible to assess short- and long-term variations in diet patterns by comparing different sections from a single feather that has progressive growing

(Thompson and Furness 1995), among feathers growing at different stages of the moult cycle

(Dalerum and Angerbjorn 2005), and analyzing feathers collected in different locations and periods of time within the species range (Kelly 2000). Feather samples can be obtained from museum specimens collected over different periods of time has providing past diet information

(Becker and Beissinger 2006).

For most tropical owl species the diet patterns and trophic relationships are poorly known

(Konig et al. 1999). Traditionally, diet composition for owls is determined mostly by observations of foraging, by stomach contents, and pellet and fecal analyses (Errington 1930, Marti 1974,

Rosenberg and Cooper 1990, Lee and Severinghaus 2004). However, identification of prey items by direct observations is difficult for nocturnal species. Analysis of stomach contents requires invasive surgery or killing of the individuals, which is not a suitable approach for rare and threatened species. Some insectivorous owls rarely produce pellets; making it difficult to study their diets (see Lee and Severinghaus 2004). Fecal analysis is limited to the number of individuals that one can capture. Therefore, using stable isotopes analysis could be a useful tool for studying diet patterns and trophic relationships in tropical owl species.

Here, I used stable isotopes analysis to ask whether diet patterns of the Bearded

Screech-Owl (Megascops barbarus) vary spatially along the species' range in the Central

Highlands of Chiapas, and temporally on short- (within and among body and rectrices feathers) and long-term periods.

The Bearded Screech-Owl is a rare and restricted endemic species in the Northern

Neotropics, and is considered threatened in Mexico and near- threatened globally (DOF 2002,

Bird Life International 2004). It inhabits montane forest from the Central Highlands of Chiapas and Central Highlands of Guatemala (Howell and Webb 1995, del Hoyo et al. 1999). Montane forests in Chiapas have been reduced to less than 25 percent of their original area with an annual

85 deforestation rate > 2.7% in the last 30 yrs (Gonzalez-Espinosa et al. 1995, Cayuela et al. 2006).

Since remaining montane forests are simplified in structure and their vegetation composition is associated with a drier and warmer forest interior (Ramfrez-Marcial et al. 2001), I predicted that if there is variation in diet over the period when the feathers were growing there will be intra- feather and inter- feather (body and rectrices) variation in stable isotopes. Furthermore, if the distribution and abundance of food types varied among regions and habitat conversion has reduced the diet quality of Bearded Screech-Owl, I would expect to find spatial and temporal differences in isotopic signatures of 513C and 515N.

METHODS

Study Area.-This study was conducted in the Central Highlands of Chiapas, Southern

Mexico (17° 11' N; 92° 53' W). The vegetation includes pine-oak, oak and cloud forests, but also patches of diverse secondary communities associated with pine-oak forests (Rzedowski 1978).

The remaining forested area covers 2 911 km2 (46%), though it has been severely fragmented

(Ochoa-Gaona and Gonzalez-Espinosa 2000).

Field and Museum Reference Feathers (Sample Collection)^- Owls were captured using a combined procedure of mist-netting and broadcasting of pre-recorded calls. Every captured owl was banded with a numbered aluminium band, weighed, and measured. Prior to release, contour feather samples (body and rectrices) were collected and stored in a paper envelope and kept at ambient temperature before analysis. The date of capture, location, and sex were recorded.

Additionally, I requested Bearded Screech-Owl contour (body) feathers from Bird Collections and

Museums Collections (Table 5.1).

Stable Isotopes Measurements.-1 removed oil and dirt from feather samples by washing them with liquid soap and then with chloroform-methanol (2:1) solution (Wassenaar and Hobson

2000). After drying at room temperature, I cut the distal end (calamus) and the upper part of each feather into small fragments and packed each part separately (0.7 - 1.1 mg) in clipping silver

86 capsules for solid samples (5x9mm; Costech, Valencia, CA, USA). When possible, pairs of body and tail (rectrices) feathers were analyzed to confirm that these feathers contained similar carbon and nitrogen isotopes ratios. Stable isotope ratios of carbon and nitrogen were measured by continuous flow isotope ratio mass spectrometry (IRMS; 20-20 mass spectrometer, PDZ Europa,

Northwich, UK) after sample combustion to CO2 and N2at 1 000 C in an on-line elemental analyzer (PDZ Europa ANCA-GSL). Gases were separated on a Carbosieve G column (Supelco,

Bellefonte, PA, USA) before introducing them to the IRMS. Sample isotope ratios were compared to those of standard gases injected directly into the IRSM before and after the sample peaks, and delta 13C (PDB) and delta 15N (AIR) values were calculated. Final isotope values were adjusted to the mean values of standard samples (a mixture of ammonium sulphate and sucrose with delta

13C= -23.83 and delta 15N= 1.33, distributed at intervals in each analytical run to the correct values of the working standards). The working standards are periodically calibrated against international isotope standards. The standard model to calculate whole sample and report the 13C and 15N in parts per mil (%o) in delta (6) notation:

SK = Rmm,,k Rslandard xlOOO R. .v tan dard

13 15 13 12 15 14 Where X is the C or N, R sampie is the ratio of C/ C or N/ N and R standard is the Pee Dee

Belemnite (PDB) standard for Carbon and AIR standard for Nitrogen. The standard deviation of the measurements for C samples was ± 0.22 %o and for N ± 0.14 %o.

Prior to statistical analysis, data residuals were checked for statistical normality with

Shapiro-Wilks (W) test and equal variance with Bartlett's test (Gotelli and Ellison 2004). I compared means of the 513C and 515N signature concentration using ANOVA or non-parametric statistical analysis. I evaluated the variation in isotopic values within feathers, between feathers of the same individual, sex, locations, and years. All statistical analyses were performed using JMP

87 IN-SAS 5.1 (Sail et al. 2005). All means are presented (± 1 SD) and tests were considered significant at a = 0.05.

RESULTS

I obtained feathers from a total of 24 individuals (12 individuals captured in the field and

12 individuals from museums) of the Bearded Screech-Owl from the highlands of Chiapas and

Guatemala. The mean of feather isotope signature values for 513C was -22.53 ± 1.29 with a range of -24.74 to -19.77%o, and mean for 515N was 5.87± 0.71 with a range of 3.96 to 7.13%o suggesting some variation in its diet. Figure 5.1 shows the distribution and correlation between stable-isotope ratios of carbon and nitrogen in body feathers (calamus) of the Bearded Screech-

13 2 15 2 Owl. There were no differences in 5 C values (X ^ 17.75, P- 0.47) and 5 N values (X 'rs=

20.2, P= 0.33) among feather samples.

Intra- and inter- feather variations in stable isotopes - Intra-body feathers (calamus and the upper part of the feathers) stable isotope analysis showed a enriched trend in assimilation

13 15 13 time in 5 C (F1i31 =3.68, P=0.06), but not in 5 N (F1i31 =0.27, P=0.6). Neither 5 C (F1|16 =

15 3.88, P = 0.07) nor 5 N (F1t 16 = 0.35, P = 0.56) showed intra-rectrices variation. There was a high and positive correlation between body and rectrice feathers in 613C (r2= 0.77, P= 0.004) and in 515N (r2 = 0.67, P = 0.01) (Fig. 5.2).

Between sex variation in stable isotopes.- There was no difference between males and females in 513C (P=0.64) and 615N (P= 0.53) isotope signatures. However females showed a wider numerical range for both isotope signatures than males. For 513C: Qmean - -22.70 ±

1.41 SD; range -24.64 to -19.77; n= 12 vs. Smean = -22AO ± 1.32SD; range -24.74 to -20.87; n =

8 and for 615N: 2 mean = 5.75 ± 0.88SD; range 3.93 to 7.13; n= 12 vs. Smean = 5.96 ± 0.44SD; range 5.30 to 6.43; n = 8.

Spatial differences in stable isotopes measurements.- Values of 513C and 515N did not vary strongly across nine locations where Bearded Screech-Owls have been recorded (Fig. 5.3).

88 However, Teopisca showed the highest values of 513C (-20.87) and 515N (6.42). Huitepec and El

Callejon showed the most depleted values of 613C (Fig. 5.3). These two locations had the highest occurrence of Bearded Screech-Owls (Chapter 2), and significant difference was observed

compared with the other sample locations (Fi,2o = 15.68, P< 0.001). No significant difference

15 was observed for6 N values (F1i20 = 2.87, P- 0.10) between these same areas. Elevation was

15 13 15 2 13 2 not related to either 5 N or 6 C values (6 N: r = 0.38, F9,12 = 0.83, P = 0.60; 5 C: r = 0.58,

F9,12= 1.84, P=0.16; Fig. 5.3).

Temporal differences in stable isotopes values.- There was no observable pattern or trend in the stable isotopes values through the years analyzed (n= 22) (Fig. 5.4). The stable isotopes in feathers collected over the years showed significant temporal differences in 615N

13 signature values (F9,12 = 4.52, P < 0.01; Fig. 5.5b), but not in 5 C values (F9i12.= 1.10, P =0.45;

Fig. 5.5a).

DISCUSSION

In order to effectively manage and conserve a threatened species, it is important to understand its diet patterns and trophic relationship with their prey. My data showed that carbon

and nitrogen isotope composition in feathers of the Bearded Screech-Owl had a range of 4.97%0 for 513C values and 3.17%o for 515N values which indicated that there was diet variations among individuals during the period of feather growth (Mizutani et al. 1990, Bolnick et al. 2003, Urton and

Hobson 2005). The range on 615N values reported for other owl species in Canada has been of

3.77%o for Northern Hawk Owl (Surnia ulula), 4.29%0 for Barred Owl (Strix varia), and 8.89%o for

Great Horned Owl (Bubo virginianus) (Duxbury and Holroyd 1997). The diets of those species

include mainly mammals but also include birds, frogs, lizards, and arthropods (Konig et al. 1999).

The Great Horned Owl, considered a generalist (del Hoyo et al. 1999), shows the highest

diversity in range of prey types in owls and also a larger range of isotope values. The wider

isotopes values reflect no specialization in the diet (Urton and Hobson 2005). Although the diet of

89 the Bearded Screech-Owl indicated some variation in the stable isotopes values, it did not have the wide range found in generalist species such as the Great Horned Owl.

The diet reported for some screech owls includes small mammals, birds, reptiles, amphibians, and fish (Gehlbach and Gehlbach 2000, Cannings and Angell 2001), but most of them eat a wide variety of arthropods where insects are the most important part of their diet

(Johnsgard 2002). The nitrogen and carbon isotope composition for the Bearded Screech-Owl was similar to that reported for an insectivorous bat species (Pteronotus parnellii: 513C= -22.41,

515N= 5.7) in tropical areas in Mexico (Herrera et al. 2001). On the other hand, the range of nitrogen isotopes values of Bearded Screech-Owl overlapped with those reported for bird species having a wider prey range (3.6-5.8%o) and also for those birds that feed exclusively on insects or small vertebrates (6-6.1%o) (Herrera et al. 2003). Fecal analysis revealed that the Bearded

Screech-Owl is mainly insectivorous and feeds mostly on Coleoptera, Orthoptera, and

Lepidoptera, but also Arachnids (Chapter 4). Based on stable isotopes values and fecal analysis, this species can be considered a prey-specialist because of its narrow range of food type (Recher

1990).

The moulting period for the Bearded Screech-Owl is prebasic (moulting after the breeding season; Pyle 1997a) and occurs during the rainy season (July through October for body feathers;

July to August for rectrices; see Chapter 4). It seems that some feathers in this species are

retained through the year. The analysis of both intra- and inter-feather (body and rectrices) to test

heterogeneity in individuals suggested no variation in diet over the period while these feathers

were growing. This implies there was no change in foraging habitat use during the period.

Contrary to the Bearded Screech-Owl, Thompson and Furness (1995) reported inter- feather

(primary feathers 2, 6, 10) variation in nitrogen and carbon in marine birds where outer feathers

(10 primary feathers) had values depleted compared with the other primary feathers. That

indicated a switch in diet over the period of primary-feather moult. However, no inter- or intra-

body (breast and back) feather variation in nitrogen and carbon was found (Thompson and

90 Furness 1995). In general, primary feathers are the largest feathers and in some bird species the replacement of these goes so slow that new moulting cycle begins before the previous ends (Gill

1990). It could be therefore better to use owl primary feathers to study diet variations. Moulting patterns in North American owl species vary substantially and certain species replace all feathers during the second prebasic moult while others take up to 6 yrs to renew all the feathers (Pyle

1997a, Pyle 1997b). For use of feathers in stable isotope studies it is important to know moulting patterns and sequence of feather development for a better interpretation of the data. Moulting pattern variation may suggest that each species has evolved a moult strategy during its annual cycle dependent on the environmental conditions in which it lives (Van de Wetering and Cooke

2000).

I found no evidence of sexual difference in the diet of Bearded Screech-Owls based on stable isotopes analysis. However, females showed a wider range in both stable isotopes measured. Carbon values in feathers in both sex showed higher variability than nitrogen values.

Hobson and Clark (1992b) reported the same higher variation in carbon for captive bird species.

Nevertheless, for wild animals the stable isotopic values showed narrower isotopic distribution

(Hobson and Clark 1992b), but the authors had no explanation for these results.

Bearded Screech-Owl's feathers reflected a terrestrial C-3 dominated ecosystem (513C

range -35 to -21; Kelly 2000). In terrestrial plant species environmental conditions can affect their carbon and nitrogen signature values, isotopes values tend to be depleted in mesic compared to xeric conditions (Marra et al. 1988). Landscape modifications by anthropogenic factors such as

urban growth, grazing, changes in agriculture techniques and selective logging for fire wood, timber and charcoal have affected the vegetation structure and floristic composition, reducing the

proportion of moist forests and increasing the isolation of the remaining moist forest fragments in the Highlands of Chiapas (Ochoa-Gaona 2001). These modifications may alter microclimatic

conditions by decreasing moisture, thus affecting both distribution and abundance of prey, which

also influences the isotopic signatures of owls, and their prey.

91 Some Screech-Owl species exhibit both spatial and temporal variations in their diets (e.g.

Eastern Screech-Owl, Gehlbach 1995; Western Screech-Owl, Cannings and Angell 2001); the stable isotopes in studied feathers of the Bearded Screech-Owl did not show spatial variation; the most depleted carbon values compared with the rest of the sampled locations were at Huitepec and El Callejon. At Huitepec the species is known only from cloud and humid oak forests

(Chapter 2); and where the relative humidity (P< 0.001) and organic matter (P <0.001) recorded in both forests has been higher compared with successional and incipient forests (Luna 2005).

The Bearded Screech-Owl is a moist forest owl in habitats where ten months of humid soil is registered (SPP 1981). In the region there is a trend to habitat fragmentation that is very variable

(Ochoa-Gaona and Gonzalez-Espinosa 2000). It is not known how many moist forest areas remain in the region and how the owl population are going in these areas.

Although the Bearded Screech-Owl's feathers showed significant temporal variation in

515N values over years (1897 to 2004), no interpretable pattern could be seen (see Fig. 5.4). The most depleted value of stable isotopes signature was of an individual captured in 1999 from the cloud forest of Huitepec (J.L. Rangel pers. comm.). Another sample with depleted 515N value also came from moist oak forest of Huitepec in 1988. A survey of the monthly mean temperature from five weather stations around San Cristobal de Las Casas for a period of 45 years showed

differences (F4171=30.63, P< 0.001) as expected for seasonal changes. However, the change in

the mean monthly rainfall over the same period was only marginal (F4171= 2.06, P= 0.08),

indicating a slight descending trend in rainfall since the early 1950s (Golicher et al. 2006). The

evapotranspiration for the same period did not show any significant (F4171=1.85, P= 0.12) changes. The Huitepec Biological Reserve is one of the last remnants of mature forest protected

in the Highlands of Chiapas (Ramirez-Marcial et al. 1998). For a long time the forests in the

Highlands of Chiapas have been transforming and reducting of the original vegetation. It is known that factors such as density of the vegetation, canopy cover, wind, and topographic conditions

influence the temperature and moistness in the interior of the forest (Kellomaki and Vaisanen

92 1997, Romero 2000). It is, therefore, likely any variation in the stable isotope values may be influenced by variations of evapotranspiration and humidity in microclimatic scales in each location and over a particular period of time. Those microclimate changes were not detectable through a review of the available data on rainfall and temperature.

The findings of this study document that the Bearded Screech-Owl is an insectivorous species in mesic habitat conditions that does not change its foraging habitat use during the period of feather growth (see Chapter 2 and 4). Although there was some temporal variation in stable isotopes analyzed, no meaningful pattern could be seen, suggesting that the stable isotopes values in this study reflected spatial rather than temporal variation in owl's diet. Individuals at Huitepec

Biological Reserve with cloud and moist oak forests showed the most depleted carbon values and also the highest owl numbers detected per linear trail (Chapter 2). In general, these data indicated that humid areas provide better habitat for survival and reproduction of owl species

(See also Ganey et al. 2005) probably because the humid oak forest at Huitepec showed higher abundance of invertebrates than other vegetation types (Chavez-Zichinelli 2002). More long-term studies and spatial dietary and prey analysis will be necessary to gain a better understanding of

how habitat conditions determine the distribution, abundance and quality of food for the Bearded

Screech-Owl.

93 5.1. Feathers used from Bearded Screech-Owl specimens located in museums and bird collections.

Museum* Date Location Lat/Long No. (sex) Collector KUNHM 3-Mar-55 13.5 Km E to San Cristobal de las Casas, Huixtan 16°43'12"N 92°30'30"W 35072 (0) R. W. Dickerman WFVZC 14-Oct-62 Finca Patichuitz, 53 Km NE Margaritas, Ocosingo 16°24'35"N 91°47'45"W 10253 (3) A. Gardner CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92°34'00"W 202 (3) M. Alvarez del Toro CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92°34'00"W 203 (3) M. Alvarez del Toro CZRAV 6-Nov-69 Entrance to Chilil trail, San Cristobal de las Casas 16°39'54"N 92°34'00"W 204 (?) M. Alvarez del Toro AMNH 12-Sep-72 8 Km to WNW from San Cristobal, Zinacantan 16°40'05"N 93°42'32"W 6959 (2) J. T. Marshall CZRAV 15-Nov-77 Close to Teopisca, San Cristobal de las Casas 16°31'00"N 92°28'60"W 205 (3) Ni** CZRAV 11-Jul-88 Huitepec Biological Reserve, San Cristobal 16°44'50"N 92°41'10"W 5158 (?) R. Vidal CZRAV Ni* Huitepec Biological Reserve, San Cristobal 16°44'50"N 92°41'10"W 5171 (3) R. Vidal CZRAV 16-Jul-93 San Jose Bacomtenelte, Zinacantan 16°43'00"N 92°42'28"W 5513 (2) M. A. Altamirano CZRAV 20-Jan-99 Huitepec Biological Reserve, San Cristobal 16°45'05"N 92°41'00"W 6542 (2) J. L. Rangel AMNH May-1897 Baja Vera Paz, Guatemala 15°06'05"N 90°19'07"W 71493 (?) A. Alfaro

*KUNHM (University of Kansas-Natural History Museum), WFVZ (Western Foundation of Vertebrate Zoology) CZRAV (Coleccion Zoologica Regional Aves-lnstituto de Historia Natural y Ecologia de Chiapas), and AMNH (American Museum of Natural History). ** Ni (No information). -19 i

-20

21 o - • • • • CO • •

S -22 -) •

-23 • -24 -I •

-25 5 6

515N (%o)

Figure 5.1. Distribution of the stable-nitrogen (15N) and carbon (13C) isotopes values from body feathers (calamus) of the Bearded Screech-Owl. Each point represents an individual owl.

95 a)

-20 -,

Figure 5.2. a) Carbon isotopes ratios of body and tail feathers from Bearded Screech-Owl (r2- 0.77, P = 0.004). b) Nitrogen isotopes ratios of body and tail feathers from the Bearded Screech- Owl (/ = 0.67; P = 0.01) collected in the Central Highlands of Chiapas, Mexico.

96 Figure 5.3. Isotopes ratios of 515N (•) and 513C (A) of body feathers from the Bearded Screech-Owl (Megascops barbarus) in nine locations in the Central Highlands of Chiapas and Guatemala. Locations are in elevation gradient (meters above sea level) from minor to major (range 1000 m), and sample size given in parenthesis. SD values given only for more than one sample.

97 -20 -,

1977- -21 1993 1969 1962 • 1955 -22 J. O CO 1972 • • 2001 "io • 1897

-23 2004

1988 -24

1999

-25 —r- 4 615N

Figure 5.4. Annual distribution of the isotope ratios of 513C and 515N of body feathers from Bearded Screech-Owl in the Central Highlands of Chiapas and Guatemala.

98 a)

-18

-20 A

o-22 CO -p • A -24 n A

-26 1890 1910 1930 1950 1970 1990 2010 Years

b)

8

LO

WD 4 H

1890 1910 1930 1950 1970 1990 2010 Years

13 15 Figure 5.5. a) Isotopes ratios of 5 C (%o) and b) Isotopes ratios of 5 N (%o) of body feathers from Bearded Screech-Owl per year (1955-2004), as well as one sample from 1897 in the Central Highlands of Chiapas and Guatemala. SD values given for years with more than one sample/yr.

99 REFERENCES

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100 Ganey, J. L, W. M. Block, J. P. Ward, Jr. and B. E. Strohmeyer. 2005. Home range, habitat use, survival, and fecundity of Mexican Spotted Owls in the Sacramento Mountains, New Mexico. Southwestern Naturalist 50: 323-333. Gannes L. Z., D. M. O'Brien, and C. Martinez del Rio. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78: 1271- 1276. Gehlbach, F.R. 1995. Eastern Screech-Owl (Otus asio). In Poole, A. and F. Gill (Eds.) The Birds of North America, no. 165. Philadelphia, PA: Academy of Natural Sciences; Washington, DC. American Ornithologists' Union. Gehlbach, F.R. and N.Y. Gehlbach. 2000. Whiskered Screech-Owl (Otus trichopsis). In A. Poole and F. Gill (Eds.) The Birds of Northern America, no. 507. Philadelphia, PA: Academy of Natural Sciences; Washington, DC. American Ornithologists' Union. Gill, F. B. 1990. Ornithology. W. H. Freeman and Company. NY, USA. Golicher, J.D., N. Ramirez-Marcial, and S. I. Levy-Tacher. 2006. Correlations between precipitation pattern in Southern Mexico and the El Nino sea surface temperature index. Interciencia 31: 80-86. Gonzalez-Espinosa, M., S. Ochoa-Gaona, N. Ramirez-Marcial, and P.F. Quintana-Ascencio. 1995. Current land use trends and conservation of old growth forest habitats in the highlands of Chiapas, Mexico. Pp. 190-198. In M. H. Wilson and S. Sader (Eds.). Conservation of Neotropical Migratory Birds in Mexico. Maine Agricultural and Forest Experiment Station.USA. Gotelli, N.J. and A.M. Ellison. 2004. A Primer of Ecological Statistics. Sinauer Assocites, Inc. Sunderland, MA, USA. Herrera, L.G., K.A. Hobson, A.A. Manzo, D.B. Estrada, V. Sanchez-Cordero, and G.C. Mendez 2001. The Role of Fruits and Insects in the Nutrition of Frugivorous Bats: Evaluating the Use of Stable Isotope Models. Biotropica 33: 520-528.

Herrera, L.G., K.A. Hobson, M. Rodriguez, and P. Hernandez. 2003. Trophic partitioning in tropical rain forest birds: insights from stable isotope analysis. Oecologia 136: 439-444. Hobson, K.A., and W. A. Montevecchi. 1991. Stable isotopic determinations of trophic relationships of great auks. Oecologia 87:528-531. Hobson, K. A. and S. G. Sealy. 1991. Marine protein contribution to the diet of the Northern Saw- whet owls on the Queen Charlotte Islands: a stable-isotope approach. Auk 108: 437-440. Hobson, K. A. and R. G. Clark. 1992a. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94: 181 -188.

101 Hobson, K. A. and R. G. Clark. 1992b. Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94: 189-197. Howell, S. and S. Webb 1995. A guide to the birds of Mexico and Northern Central America. Oxford University Press. California, USA. Johnsgard, P.A. 2002. North American Owls. 2nd Ed. Smithsonian Institution Press. Washington. USA. Kellomaki, S. and H. Vaisanen. 1997. Modelling the dynamic of the forest ecosystem for climate change studies in boreal conditions. Ecological Modeling 97: 121-140. Kelly, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78: 1-27. Konig C, F. Weick, and J-H Becking. 1999. Owls. A guide to the owls of the worlds. Yale University Press. USA. Lee, Y.F. and L. L. Severinghaus. 2004. Sexual and seasonal differences in the diet of Lanyu Scops Owls based on fecal analysis. Journal of Wildlife Management 68: 299-306. Luna, C. J. 2005. Distribucion, abundancia y diversidad de Curculionidae (Insecta: Coleoptera) de hojarasca en la Reserva Huitepec, Chiapas, Mexico. M.Sc. Thesis. El Colegio de la Frontera Sur. Chiapas, Mexico. Marra, P.P., K.A. Hobson, and R.T. Holmes. 1998. Linking winter and summer events in a migratory bird by using stable- carbon isotopes. Science 282: 1884-1886. Marti, C. D. 1974. Feeding ecology of four sympatric owls. Condor 76: 45-61. Mizutani, H., M. Fukuda, and E. Wada. 1990. Carbon Isotope ratio of feathers reveals feeding behavior of Cormorants. Auk 107: 400-437. Ochoa-Gaona, S. 2001. Traditional Land-use systems and patterns of forest fragmentation in the Highlands of Chiapas, Mexico. Environmental Management 27: 571-586. Ochoa-Gaona, S. and M. Gonzalez-Espinosa. 2000. Land use patterns and deforestation in the highlands of Chiapas, Mexico. Applied Geography20:17'-42. Pyle, P. 1997a. Identification guide to North American Birds. Part 1 Columbidae to Ploceidae. Slate Creek, Bolinas CA. USA. Pyle, P. 1997b. Flight-feather molt patterns and age in North American Owls. Monographs in Field Ornithology No. 2. American Birding Association. CO, USA. Ramirez-Marcial, N., S. Ochoa-Gaona, M. Gonzalez-Espinosa, and P. F. Quintana-Ascencio. 1998. Analisis florfstico y sucesional en la Estacion Biologica Cerro Huitepec, Chiapas, Mexico. Acta Botanica Mexicana 44: 59-85.

102 Ramfrez-Marcial, N., M. Gonzalez-Espinosa, and G. Williams-Linera. 2001. Anthropogenic disturbance and tree diversity in montane rain forest in Chiapas, Mexico. Forest Ecology and Management 154: 311 -326. Recher, H. F. 1990. Specialist and generalist: avian response to spatial and temporal changes in resources. Pp. 333-336. In M.L. Morrison, C. J. Ralph, J. Verner, and J. R. Jehl Jr. (Eds.). Studies in Avian Biology 13. Cooper Ornithological Society. Romero Najera, I. 2000. Estructura y condiciones microambientales en bosques perturbados de los Altos de Chiapas, Mexico. B.Sc. Thesis. Universidad Nacional Autonoma de Mexico. Mexico, D.F. Rosenberg, V. and R. J. Cooper. 1990. Approaches to avian diet analysis. Pp. 80-90. In M.L. Morrison, C. J. Ralph, J. Verner, and J. R. Jehl Jr. (Eds.). Studies in Avian Biology 13. Cooper Ornithological Society. Rzedowski, J. 1978. Vegetacion de Mexico. Limusa, Mexico, D. F. 432p. Sail, J., L. Creighton and A. Lehman. 2005. JMP Start Statistics. SAS Institute Inc. 3th Ed. SAS Institute Inc. Thompson Learning, Belmont, California, USA. Secretaria de Programacion y Presupuesto (SPP). 1981. Carta de humedad en el suelo. Escala 1:1 000 000. Villahermosa. Direccion General de Geograffa. SPP. Mexico, D. F. Thompson, D.G. and R.W. Furness. 1995. Stable-isotope ratios of Carbon and Nitrogen in feathers indicate seasonal dietary shifts in Northern Fulmars. Auk 112: 493-498. Urton E.J.M. and K. A. Hobson. 2005. Intrapopulation variation in gray wolf isotope (515N and 5 13C) profiles: implications for the ecology of individuals. Oecologia 145: 317-326. Van de Wetering, D. and F. Cooke. 2000. Body weight and feather growth of male barrow's golden eye during wing molt. Condor 102: 228-231. Wassenaar, L. I., and K. A. Hobson. 2000. Stable-carbon and hydrogen isotope ratios reveal breeding origins of Red-winged Blackbirds. Ecological Applications 10: 911-916.

103 CHAPTER 6:

SUMMARY AND CONCLUSIONS

My thesis research examined aspects of distribution, abundance, habitat selection, natural history and diet of the endemic, threatened Bearded Screech-Owl (Megascops barbarus) from the tropical montane forest in the Central Highlands of Chiapas, Mexico. I provided key information to understand the environmental conditions and ecological requirements for the survival of this species within a continuing environmental of human-induced change in the region.

BEARDED SCREECH-OWL (ENDEMIC OWL OF TROPICAL MONTANE FORESTS)

In my survey, the small number of Bearded Screech-Owls encountered in nine locations

(1.65±0.61 owls/Km of trail) in the Central Highlands of Chiapas confirmed their rare species status (see Chapter 2). However, the number of owls varied spatially and they are more likely to be detected in humid forests. Important forest types associated with the owls' presence were humid pine-oak forests, cloud forest and humid oak forest, though owl presence was also recorded in perturbed pine forest habitats. It therefore appears that Bearded Screech-Owls are able to utilize disturbed forests as long as they are associated with or nearby old growth forests.

Similarly, habitat edges were also utilized as roosting areas. This might suggest that the species can benefit from edge effects associated with habitat fragmentation, as has been reported for the

Spotted Owl (Strix occidentalis) in north-western USA (Franklin et al. 2000). On the other hand, I identified predation and slingshot hunting as major causes of mortality for the Bearded Screech-

Owl (see Chapter 3). Predation has been considered as having a great impact in owl communities (Hakkarainen and Korpimaki 1996), and owls could also be more exposed to predators along straight edges when they utilize them as roosting sites. Furthermore, owls would be more exposed to hunting along edges. Never the less, a mosaic of vegetation types in the landscape dominated by old growth forest may provide optimal conditions for the reproduction and survival of the Bearded Screech-Owl at the regional scale. 104 At the Huitepec Biological Reserve, I recorded the highest owl number (3.37 ± 0.36 owls/Km). This reserve maintains protected old-growth and secondary forests with edges, and represents the conditions described in the previous paragraph that would support a higher owl population. The rest of the studied locations, which present different levels of human disturbance, recorded much lower owl occurrence. The Huitepec Reserve may be the only breeding site for the Bearded Screech-Owl in the area; the only nest found was located in the reserve. This reserve has been considered one of the last protected remnants of mature forest in the Central

Highlands of Chiapas and my research findings emphasized the importance of the Huitepec

Reserve for the breeding and survival of the Bearded Screech-Owl.

The habitat attribute that appeared to have a strong influence on the occurrence of the

Bearded Screech-Owl was the amount of canopy cover. Canopy cover maintains good microclimatic conditions such as humidity and temperature in the interior of the forest (Romero

2000). Canopy cover also provides protection against predators (Ward et al. 1998) and provides roosting and nesting sites for owls (e.g. Spotted Owl, S. occidentalis, Ganey et al. 1999). Another important habitat attribute associated with Bearded Screech-Owls occurrence was steep slope

(40.34% ± 5.28). In the Highlands of Chiapas, steep slopes with northwest aspects are more humid to maintain better vegetation conditions (Ramirez-Marcial et al. 1998) that may facilitate the survival and reproduction of the owl. They are also found in areas away from human activity.

The habitat attributes associated with Bearded Screech-Owls indicated that this species is a habitat specialist adapted mainly to humid pine and oak forests.

The home range sizes recorded for Bearded Screech-Owls were similar to other small forest insectivore owls such as the Flammulated and Western Screech-Owls (McCallum 1994,

Cannings and Angell 2001). There was a larger variation of home range sizes in El Callejon compared with the Huitepec. At El Callejon, local people selectively harvest branches or trees for firewood or timber, resulting in more variations of the undergrowth in the area. Human disturbances in this managed area, even though moderate, could cause the larger observed

105 home range sizes as owls may need to expand their home ranges to meet their diet and other habitat needs. However, other interacting factors such as age and breeding season could not be ruled out.

In addition to habitat studies, I also examined the breeding and foraging biology of the

Bearded Screech-Owl. Similar to most other owl species, the Bearded Screech-Owl showed reversed sexual dimorphism, females being heavier and had longer tail than males, but smaller tarsus and culmen. Several hypotheses have been proposed to explain the reverse sexual dimorphism in owls (Earhart and Johnson 1970, Mueller 1986). All these hypotheses can be grouped into three categories: (1) ecological hypotheses, (2) sex-role differentiation hypotheses, and (3) behavioral hypotheses. The ecological hypotheses share the premise that reversed sexual dimorphism has evolved to permit the sexes to capture different sizes of prey, thus reducing competition between the sexes and allowing a pair to exploit a wider range of sizes of prey (Earhart and Johnson 1970). The sex-role differentiation hypotheses permit the sexes to perform better in various activities associated with reproduction. For instance, large females can lay larger eggs than smaller individuals but also large females are more effective in deterring predators than smaller individuals (Storer 1966). The behavioral hypotheses hold that reversed sexual dimorphism has evolved to facilitate female dominance of the male (Mueller

1986). However, there are not enough ecological and behavioural information about the Bearded

Screech-Owl to determine which hypothesis this owl would fit in.

I found the first nest for the Bearded Screech-Owl in a natural cavity of an old oak tree

(Quercus laurina) in the Central Highlands of Chiapas. This tree species is one of the dominant oaks in moist habitats (Gonzalez-Espinosa et al. 1995). Screech owls are obligate secondary cavity nesters and depend on the availability of suitable cavities for nesting. The availability of cavities for nesting increases in old forests with the age of the trees (Newton 1998), but the

Highlands of Chiapas have been exposed to selective logging and the availability of natural

106 cavities may be a limiting factor for owls nesting in the region. Thus, it will be essential to keep stands of old trees with natural cavities to provide nesting sites for the Bearded Screech-Owl.

Diet analysis showed that the Bearded Screech-Owl eats mostly arthropods. Feces analysis indicated that beetles (Melonontidae-Coleoptera), crickets (Orthoptera), moths

(Lepidoptera), and spiders (Arachnids) represent the diet of this small owl. Additionally, stomach contents from two museum specimens collected in the region included cockroaches, caterpillars, and scorpions (Museum notes). The stable isotopes analyses confirmed that this species is insectivorous in mesic habitats conditions. These analyses indicated that there were not diet variations among individuals during the period of feather growth, but there were no significant spatial variation in the use of foraging habitat. While my findings seem to indicate that the

Bearded Screech-Owl is an invertebrate food specialist with a narrow range of species consumed, further research in dietary characteristics and prey availability is necessary to better understand the temporal dietary variations over a long-term period.

After three field seasons, I recorded 54 individuals within an area of 4 000 km2 and encountered just one nest. Thus, my results support that the species is quite rare and uncommon. Although they may benefit from forest edges created by fragmentation, overall they seem to be highly susceptible to habitat loss and degradation. The population ecology of the

Bearded Screech-Owl fits the small-population paradigm (Caugley 1994). At the same time, it is also a species with 'slow' life histories (high survival rates, low reproductive rates). As such, they would be more vulnerable to changes of environmental conditions (Owens and Bennett 2000). It is crucial to have a better understanding of the interaction between population size and demographic characteristics before one can predict how the Bearded Screech-Owl population will fare with imminent habitat fragmentation and degradation of forests.

107 CONSERVATION ECOLOGY OF THE BEARDED SCREECH -OWL IN THE MONTANE FORESTS OF CHIAPAS

Although Neotropical areas support high owl diversity, our knowledge of Neotropical ecology is very limited (Enriquez et al. 2006). In Chiapas, owls are one of the avian groups requiring more research (Rangel-Salazar et al. 2005). The Bearded Screech-Owl is listed as threatened by the Mexican Government (DOF 2002) and near threatened by the IUCN (Bird Life

International 2004) because of the lack of ecological and biological knowledge about this bird, and the fragmentation of tropical montane forests where it inhabits. Although my thesis research has only briefly examined the distribution, habitat association, morphology, and diet of the

Bearded Screech-Owl, and even though the data presented here are limited by sample size, it was the important first step taken towards understanding the conservation ecology of this threatened species.

In the Central Highlands of Chiapas the estimated annual deforestation rates from 1974-

1984 and from 1984-1990 were 1.58 and 2.13%, respectively (Ochoa-Gaona and Gonzalez-

Espinosa 2000). Forest fragmentation and habitat degradation are considered the most severe threat to conservation of raptors in the tropics (Thiollay 1985). However, these invasive processes may have different effects on the species composition of raptor assemblage. Human disturbances may affect diversity mostly at the local level (Willis and Whittaker 2002). Reducing the natural growth and regeneration from the forest interior and canopy trees, there is often a local increase in distribution of pines over oaks, causing a loss in diversity of canopy trees and understory shrubs. An associated effect is the loss in soil fertility (Gonzalez-Espinosa et al. 1991, Ramirez-

Marcial et al. 2001). As mentioned in Chapter 3, canopy cover and understory tree species diversity and density decrease as human disturbance increases in Chiapas (Ramirez-Marcial et al. 2001). The canopy cover was found to be one of the most important habitat attribute associated with the occurrence of Bearded Screech-Owl (see Chapter 3). In areas with human

disturbance, the reduction of canopy cover may have negatively affected the abundance and

distribution of this owl species in the region. Therefore, restoration programs in degraded areas

108 by planting native trees and bushes in different successional conditions would likely increase the habitat availability for the Bearded Screech-Owl in the region. With restricted distribution and it being a habitat specialist to humid pine-oak forest, the Bearded Screech-Owl would be very sensitive to extensive and intensive changes in land use occurring in the region.

The levels of perturbation in forests of the Central Highlands of Chiapas vary in patterns of intensity and frequency with the land use history, environmental, and socioeconomic attributes at each site (Ochoa-Gaona 2001). For instance, the traditional forest use has a high frequency perturbation of moderate intensity (Barron-Sevilla 2002). Conservation efforts for this threatened mountain owl should therefore consider perturbation factors both at the local and the regional levels.

Installation of nest boxes has increased the local breeding densities of cavity nesting birds (Newton 1998). Nest boxes program for the Bearded Screech-Owl would be a way to increase nest site availability and breeding success. However, the availability of natural cavities for nesting should be better assessed before any nest box program is started.

FUTURE RESEARCH ON THE BEARDED SCREECH-OWL

Priority for future research on this endemic Screech-Owl should be obtaining detailed information on the breeding ecology, life history strategies, demography, and population trends to evaluate the conservation status of this threatened owl species. It is also important to understand

how habitat changes are affecting the owl's survival by evaluating habitat connectivity (Harris et al. 2005). To develop a long-term conservation strategy, it is essential to gather information on temporal and spatial variation of ecological processes (e.g., predator-prey interactions, competition, and Juvenal dispersion). Finally, conservation efforts would only be effective if the widespread habitat degradation can be drastically reduced and eventually reversed.

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