CHIROPTERAN DIVERSITY AND ECOLOGY

IN APANAMANIAN CLOUD FOREST

by

Angela J. Aarhus

A Thesis submitted in partial fulfillment of the requirements of the degree MASTER OF SCIENCE IN NATURAL RESOURCES (WILDLIFE) College of Natural Resources UNIVERSITY OF WISCONSIN Stevens Point, Wisconsin

May2002 APPROVED BY THE GRADUATE COMMITTEE OF:

Dr. Eric M~erson, Committee Chairman Professor of Wildlife Ecology University of Wisconsin - Stevens Point

Professor of Wildlife University of Wisconsin - Stevens Point

Dr. Hans G. Schabel Professor of Forestry Coordinator of Master's Internationalist Program University of Wisconsin - Stevens Point

ii Abstract

Habitat preference and vertical stratification were determined for bats (order

Chiroptera) residing in the cloud forests of Parque Internacional La Amistad m

Western Panama. Between June and November 2001, bats were captured m understory and canopy mist nets placed across streams, trails, and forest gaps in both primary (3 sites) and secondary (3 sites) cloud forest habitat. Sampling took place during the wet season for a total of 56 nights or 2548 mist net hours (mnh). In all,

11 73 bats were captured, representing 15 species, two families, and ten genera.

Diversity for the entire La Amistad bat community was estimated at H' = 1.58. Five phyllostomid species, Anoura geoffoyi, Sturnira hondurensis, Artibeus aztecus,

Sturnira mordax, and Artibeus toltecus accounted for more than 98% of all captures and were present throughout the study period. Monthly capture rates for these common species varied over the wet season. At times of high abundance, large numbers of reproductively active females were observed for S. hondurensis, S. mordax, and A. geoffroyi. In the nectarivore, A. geoffroyi, this peak coincided with a time when flowers of the Majaguillo (Heliocarpus popayanensis) were abundant in the study area. Species diversity did not differ significantly between disturbed and undisturbed sites, however bats were substantially more abundant in secondary forest

(58.4 captures per 100 mnh) than primary forest (23.6 captures per 100 mnh). Three of the five common species, A geoffroyi, S. hondurensis, and A. toltecus, preferred secondary forest, while the remaining two occurred in both forest types equally.

Vertical stratification by bat species was biased to the canopy where 78% of all captures occurred. All common species were significantly more abundant at the

iii canopy level, except for the frugivore S. mordax, which was captured equally in understory and canopy nets. Analysis of the La Amistad bat community via a feeding guild/body size niche matrix revealed that only five of the ten possible feeding guilds were represented in La Amistad and suggested that medium-sized members of the frugivore guild might be minimizing competition by using different food types and activity times. Habitat generalism in S. mordax may be a mechanism by which this species minimizes competition with its numerically dominant congener S. hondurensis for access to highly nutritious but patchily available Solanum fruits.

Overall, this research suggests that bat species residing at high elevations might be generalists, capable of existing in both disturbed and mature cloud forest habitat, and might be coupling their energetically costly reproductive activities with local peaks in resource abundance.

iv Restimen

Se determin6 la preferencia por el habitat y el estrato vertical de los murcielagos

(orden Chiroptera) que habitan en los bosques nubosos del Parque Internacional La

Amistad en el oeste de Panama. Entre junio y noviembre de 2001 se capturaron los murcielagos con redes de neblina colocadas a nivel del sotobosque y del dosel del bosque en riachuelos, senderos y claros de un bosque primario (3 sitios) y de un secundario (3 sitios). Se muestre6 durante la estaci6n lluviosa por un total de 56 noches o 2548 horas-red. En total se capturaron 1173 murcielagos pertenecientes a

15 especies, dos familias y dies generos. La comunidad de murcielagos mostr6 un valor de diversidad de H'= 1.58. Cinco especies de filost6midos, Anoura geoffroyi,

Sturnira hondurensis, Artibeus aztecus, Sturnira mordax y Artibeus toltecus, representaron mas del 98% de las capturas y estuvieron presentes durante todo el estudio. La tasa de captura mensuales para estas especies comunes variaron durante la estaci6n lluviosa. Durante la epoca de gran abundancia muchas hembras reproductivas fueron observadas en S. hondurensis, S. mordax y A. geoffroyi. Para el nectarivoro, A. geojfroyi, su gran abundancia coincidio con un periodo de floraci6n de majaguillo (Heliocarpus popayanensis) en el area perturbado del estudio. Los indices de diversidad no difirieron significativamente entre el bosque perturbado y no perturbado, aunque habian mas capturas en el bosque secundario (58.4 capturas / 100 horas-red) que en el bosque primario (23.6 capturas / 100 horas-red). Tres de las

cinco especies comunes, A. geoffroyi, S. hondurensis y A. toltecus prefirieron el

bosque secundario, mientras que las otras dos ocurrieron igualmente en ambos

bosques. La estratificaci6n .vertical de los murcielagos fue sesgada hacia el nivel del

V dosel, en donde el 78% de las capturas se realizaron. Todas las especies comunes fueron significativamente mas abundantes en el dosel, excepto el frugivoro S. mordax, el cual fue capturado igualmente en el sotobosque y en el dosel. El analisis de la comunidad de murcielagos de La Amistad con una matrix de nichos de los gremios alimenticios y la masa corporal revel6 que solamente cinco de los dies gremios alimenticios estuvieron representados en La Amistad y sugirio que los miembros con tamafio medio dentro del gremio de frugivoros pueden minimizar la competencia al consumir diferentes tipos de alimentaci6n y estar activqs a diferentes horas. La generalizaci6n en el uso del habitat por S. mordax puede ser un mecanismo para reducir la competencia con su congenerico mas abundante S. hondurensis por el acceso a las frutas nutritivas de Solanum con su distribuci6n en parches. Sobre todo, esta investigaci6n sugiere que los murcielagos de las tierras altas son generalistas por su capacidad de existir tanto en un bosque nuboso perturbado como no perturbado y que ellos realizan sus costosas actividades reproductivas durante los periodos de maxima abundancia en recursos locales.

vi ACKNOWLEDGMENTS

First and foremost, I acknowledge with sincere thanks the community of Las

Nubes for opening their hearts and homes to me and making my two years in the

Peace Corps a powerful and unforgettable experience. I am extremely grateful to my field assistants Deibys and Carlos Fonseca for their enthusiasm, hard work, and dedication. I thank volunteers from the community ecotourism group AS.A.E.L.A.

(Asociaci6n Agro-Ecoturistica La Amistad) and other friends who assisted with field research, especially Diogenes Patifio, Mayanin Ortiz, and Nie Enstice. I am grateful to A.N.A.M. (Autoridad Nacional del Ambiente) for permission to study the bats in

La Amistad, as well as the rangers of La Amistad International Park for recording daily temperature and precipitation information, especially Antonio Gallardo and

Domingo Jurado. I am thankful to Bat Conservation International, the Zoological

Society of Milwaukee County, and the Student Research Fund of the University of

Wisconsin, Stevens Point for funding this research. I express my sincere thanks to my graduate committee chair, Dr. Eric Anderson for his guidance and support over the past four years, and especially with study logistics while I was in Panama and data analysis, and to my graduate committee, Dr. James Hardin and Dr. Hans Schabel for their comments on my thesis. I am especially indebted to Dr. Rafael Samudio Jr. of the University of Florida, Gainesville and the Smithsonian Tropical Research Institute for his invaluable collaboration and encouragement throughout all phases of my research from study logistics to data interpretation, for sharing his extensive knowledge of tropical bats with me, and above all for inspiring me with his interest and commitment to studying and protecting la naturaleza bellisima de Panama. I am

vii very thankful to my family for their unconditional support, especially my mom. And above all, I am forever grateful to my best friend Matthew Ward for his incredible support, encouragement, and dedication throughout this roller coaster experience.

viii FOREWARD

This thesis summarizes the research I performed while serving as a U.S. Peace

Corps volunteer in the Republic of Panama from December 1999 to December 2001.

Its purpose was to provide insight into the diversity and ecology of the mountain bat population residing in Parque Internacional La Amistad, in particular how its members organize themselves with respect to each other and limited resources available in this highland community. This study provides baseline information from which park management strategies for bat conservation may be developed and future scientific studies may be designed to fill in the gaps in our current understanding, particularly with regards to the demography and foraging ecology of highland bat communities.

ix TABLE OF CONTENTS

ABSTRACT ...... iii

ACKNOWLEDGMENTS ...... vii

FORWARD ...... ix

LIST OF TABLES ...... xii

LIST OF FIGURES ...... xiii

LIST OF APPENDICES ...... xiv

WTRODUCTION ...... 1

STUDY OBJECTIVES ...... 8

STUDY AREA ...... 9

METHODS ...... 12

Mist Net Sampling ...... 12

Data Analysis ...... 13

RESULTS ...... 16

Diversity, Richness, and Abundance of La Amistad Bats ...... 16

Temporal Distribution of La Amistad Bats ...... 19

Monthly Activity Patterns ...... 19

Nightly Activity Patterns ...... 19

Spatial Distribution of La Amistad Bats ...... 24

Primary versus Secondary Cloud Forest ...... 24

Vertical Stratification ...... 26

X Composition and Structure of La Amistad Bat Community ...... 30

Reproductive Ecology of La Amistad Bats ...... 34

DISCUSSION ...... 41

Temporal Distribution of La Amistad Bats ...... 41

Spatial Distribution of La Amistad Bats ...... 47

Composition and Structure of La Amistad Bat Community ...... 50

Reproductive Ecology of La Amistad Bats ...... 59

CONCLUSIONS ...... 64

LITERATURE CITED ...... 67

APPENDICES ...... 75

xi LIST OF TABLES

I. Total number of captures for bat species in La Amistad ...... 18

2. Total bat species richness, abundance, and diversity in La Amistad ...... 25

3. Vertical stratification by La Amistad bats ...... 28

4. Guild designations, mean weights (g), and mean forearm lengths (mm) for La Amistad bat species ...... 31

5. Niche matrix for La Amistad bat community ...... 32

6. Sex and age distribution for La Amistad bat species ...... 36

xii LIST OF FIGURES

1. Map of study area: Parque Internacional La Amistad, Panama ...... 10

2. Cumulative species curve for La Amistad bat community ...... 17

3. Monthly capture rates for the five most common phyllostomid species captured in La Amistad ...... 20

4. Nightly flight activity for five most common phyllostomid bat species in La Amistad between June and November 2001 ...... 21

5. Nightly flight activity for three common phyllostomid bat species during October 2001 ...... 22

6. Presence of five most common phyllostomid bat species in primary and secondary cloud forests of La Amistad ...... 27

7. Reproductive condition of adult females of three common phyllostomid bat species by month in La Amistad ...... 35

8. Percentage of adult and subadult individuals of three common phyllostomid bat species captured by month in La Amistad ...... 38

9. Sex distribution for common phyllostomid bat species in La Amistad ...... 39

xiii LIST OF APPENDICES

1. Mean minimum and maximum temperatures and total _rainfall in Parque Internacional La Amistad for 2001 ...... 76

2. Monthly species diversity, richness, and abundance for La Amistad bat community between June and November 2001 ...... 77

3. Presence / absence of La Amistad bat species between June and November 2001 ...... 78

4. Monthly species diversity and richness in primary and secondary cloud forests of La Amistad ...... 79

5. Presence of La Amistad bat species in primary and secondary cloud forests of La Amistad between June and November 2001 ...... 80

6. Vertical stratification of bat species in primary and secondary cloud forests of La Amistad ...... 81

7. Mean weights (g) and forearm lengths (mm) for male and female individuals from La Amistad bat species ...... 82

8. Reproductive condition of adult females of 15 La Amistad bat species by month...... 83

xiv INTRODUCTION

Accounting for approximately one-fourth of the world's 4,200 extant mammal species, bats (order Chiroptera) form one of the largest and most diverse mammal orders in existence, second only to the rodents (order Rodentia} in species richness

(Findley 1993). Largely due to their ability to fly, bats are also among the most widely distributed of all mammals, with a range that crosses all continents except

Antarctica and reaches its greatest diversity in the tropics (Kunz and Pierson 1994).

As pollinators and seed dispersers, bats play a pivotal role in structuring and maintaining tropical forest communities, while insectivorous species serve to regulate nocturnal insect populations, including important agricultural pests (Kunz and Pierson

1994). Loss of roosting and foraging habitats, due to deforestation and pesticide contamination, seriously threaten the future of bat populations throughout the world, especially vulnerable species with restricted geographic ranges or specialized roosting or feeding requirements (Kunz and Pierson 1994). Research that studies the effect of habitat disturbance on bat diversity by documenting the relationship between species commonly associated with undisturbed, primary forest habitat and those more typically found in disturbed, second growth habitats is essential for the development of management practices aimed at conserving these keystone species (Wilson et al.

1996).

Studies designed to understand better the local distribution patterns and species-habitat associations in tropical regions have focused largely on the highly diverse lowland bat communities. For instance, lowland studies have documented an important relationship between bat species richness and habitat disturbance level, 2 such that undisturbed, primary forests tend to harbor greater numbers of species than disturbed habitats (Fenton et al. 1992, Brosset et al. 1996, Vaughan and Hill 1996,

Wilson et al. 1996). Research of this type is essential to bat conservation because it identifies habitats most critical for the survival of different bat species by identifying species with specific habitat requirements (Vaughan and Vaughan 1986), as well as those which display habitat plasticity, or the ability to live in a broader range of habitats with varying degrees of disturbance (Estrada et al. 1993). A few studies have attempted to quantify the relationship between habitat disturbance and bat diversity by using the density of certain phyllostomid species, such as foliage-gleaning insectivorous bats, to indicate the level of disturbance in a particular habitat (Wilson et al. 1996, Fenton et al. 1992, and Medellin et al. 2000, Schulze et al. 2000). Little is known as to whether these relationships hold across altitudinal levels, due to a paucity of similar studies of highland bat communities. One high elevation study available for comparison comes from Monteverde (1400-1600 m) in Costa Rica and suggests that habitat disturbance indeed may not produce a noticeable difference in the bat species assemblages encountered in primary and secondary growth premontane forests (LaVal and Fitch 1977).

Elevation plays a fundamental role in the structure of bat communities.

Several studies looking at diversity patterns along an elevational gradient have found that bat diversity is greatest in the lowlands and decreases with altitude (Graham

1983, Mufi.oz Arango 1990, Patterson et al. 1996, Patterson et al. 1998), regardless of season (Sanchez-Cordero 2001 ). When compared to lower elevations, highland bat communities display a significant reduction in species richness accompanied by a 3 high degree of taxonomic and trophic simplicity (Soriano 2000). According to

Patterson et al. (1996), only three of 16 families of New World bats (Phyllostomidae,

V espertilionidae, and Molossidae) have been found to exist at high elevations and interestingly they are the same ones whose ranges extend northwards into the temperate region. As is the case with higher latitudes, reductions in temperature, habitat complexity, and food availability present a unique set of demands on bat species living at high elevations which might act either independently or cumulatively to reduce significantly bat diversity at higher altitudes (Graham 1983, Munoz Arango

1990).

Habitat complexity, as defined by the level of vertical stratification and patchiness within a habitat, is thought to influence positively species diversity, due to the greater number of potential niches (e.g., roosts) available in a more structurally complex habitat (August 1983). Along an elevational gradient in the Andes of Peru, habitat complexity was greatest in the lowlands and decreased with altitude (Terborgh

1977). In Colombia, Sanchez-Palomino et al. (1996) found a strong correlation between the large value for species diversity and the high- complexity of the lowland riparian habitat in Serrania La Macarena. When comparing the pre-montane cloud forests of Monteverde with two lowland sites in Costa Rica, LaVal and Fitch (1977) found bat diversity to be lowest in the highland forest and related this to a reduction in the structural complexity of the forest occurring at the higher elevation.

Constant low temperatures place enormous demands on bat species residing at high elevations. The physiological stresses to highland bats, associated with the high energetic cost of thermoregulation, directly might threaten their overall fitness 4

(survival and reproductive success) and might prevent the immigration by lowland species even if niche space is available (Graham 1983). According to Soriano (2000), the enormous loss in species diversity at high elevations might be due to the inability of a great many insectivorous species (75% reduction at higher elevations) to thermoregulate efficiently due to the metabolic limitations imposed by a high protein, low carbohydrate diet.

Thirdly, lower species diversity in highland bat communities may be a response to reductions in food productivity. According to Graham (1983), reduced light intensity with greater cloud cover, low temperatures, and permanently high humidities in highland regions likely produce a level of food abundance incapable of supporting the density of bats found in the lowlands. He further postulated that bat species residing at high elevations might be expected to take advantage of a wider range of patchily available resources (e.g., fruits, nectar, insects) to improve their overall fitness, especially during energetically costly activities, such as reproduction.

Highland bat assemblages are thought to be comprised merely of subsets of those species occurring at lower elevations, thereby lacking replacement by high elevation specialists (Patterson et al. 1996, Patterson et al. 1998, Utzurrum 1998).

Patterson et al. ( 1996) argue that most highland bat species exhibit a broad elevational range due their ability to tolerate high climatic variation and resource scarcity. One such highland resident is the nectarivore Anoura geoffroyi whose elevational range extends from 700 m to as high as 3600 m. Nectarivores such as this possess very high metabolic rates, made possible by a diet rich in carbohydrates, which allow them to 5 maintain a stable body temperature despite variation in ambient temperature (Soriano

2000).

While altitudinal overlap may be the case with many highland bat species, several cases of elevational replacement have been recorded, especially in the genera

Sturnira and Carollia (Koopman 1978, Kalko et al. 1996, Mufi.oz Arango 1990,

Giannini 1999, Soriano 2000). In the Andes of Argentina, for example, the elevational distribution of two sympatric frugivores, Sturnira erythromos and Sturnira

!ilium appear to coincide with the altitudinal availability of their preferred fruit types,

Solanum in the highlands and piper in the lowlands (Giannini 1999). Species of these genera have been classified as sedentary frugivores or bats that specialize on local plants with year-round fruit production, but providing only a few ripe fruits per night

(Soriano 2000). Nomadic frugivores, on the other hand, are those which must move to different regions to feed on temporarily abundant preferred foods from trees with explosive, short-term fruit production (Soriano 2000). One such example is Artibeus lituratus, a common resident in lowland areas that has been observed tracking fig abundance fruiting sporadically along an elevational gradient (Timm and LaVal

2000).

Conservation of large connected blocks of suitable habitat along elevational gradients may be essential for the survival of numerous altitudinal migrants.

Movement patterns in fruit-eating birds suggest that altitudinal migrants may be tracking food sources based on their spatio-temporal availability (Loiselle and Blake

1991 ). The availability, abundance, and distribution of resources, such as food and roosts, are important contributors to the structure and demography of bat communities 6 occurring at both high and low elevations (Kalko et al. 1996). More information is needed on the role resource exploitation plays on the daily or seasonal movements by bats, which influence the organization and dynamics of bat assemblages at various elevations (Patterson et al. 1998).

While highland bat communities may not represent geographical hot spots with respect to bat species richness, they are important conservation areas for several reasons. First, endemic species may be more common at higher elevations (Patterson et al. 1998, Sanchez-Cordero 2001). In the small Central American Republic of

Panama, what little research that has been performed in highland areas has identified several endemic species, such as Sturnira mordax (R. Samudio Jr., Smithsonian

Tropical Research Institute, unpublished data). This species has a restricted range and is found only in middle to high elevation forests located in Panama and Costa Rica

(Arita and Ortega 1998, Reid 1997). Continued research is essential for the identification and protection of other endemic species of bats residing at these higher elevations.

Highland bat species may be at greater risk due to both natural and human­ induced variables, influencing mountain communities. For instance, the reduced geographic area available at higher elevations combined with the stressful thermal environment might cause extinction rates to be higher than those in lowlands, leading to the greater likelihood of a natural catastrophe extirpating a highly vulnerable highland bat population (Graham 1983). Also, greater development pressures in montane regions may threaten bat populations by altering important foraging and roosting habitats. In the highlands of Panama, rich volcanic soils and cool 7 temperatures make the land highly suitable for vegetable and coffee production and have led to wide-scale deforestation and the under-regulated use of pesticides

(Samudio 2001).

A scarcity of community inventories at high elevations prevents our understanding the factors shaping tropical mountain bat communities. As in other tropical areas, most bat researchers in Panama have focused on the composition

(number and types of species) and structure (how members partition the available resources, such as roosts and food) of rich lowland bat communities (McNab 1971,

Fleming et al. 1972, Kalko et al. 1996). On Barro Colorado Island in the Panama

Canal, for example, intense, long-term monitoring of the bat community since 1908 has revealed a rich fauna, represented by 66 of the 114 bat species that have been recorded nationwide (Kalko et al. 1996). Highland bat communities in Panama have not been adequately studied, however. It has been postulated that as diversity decreases with elevation, specialist species drop out of communities and generalists persist (Fleming 1986b). Further research is necessary to study how the composition and structure of bat communities in Panama change with elevation and whether species with generalist strategies, such as the ability to survive in habitats with varying degrees of disturbance, are indeed more common at higher elevations than habitat specialists. 8

STUDY OBJECTIVES

My primary research objective was to determine the relationship between highland bat diversity (species richness and abundance) and habitat disturbance in the primary and secondary cloud forests of La Amistad International Park in Western

Panama. Additional objectives were to document the composition and structure of this highland bat community in terms of species diversity, richness, and abundance, vertical stratification, and feeding guilds and to describe the reproductive ecology of highland bat species during the wet season of 2001. The baseline information acquired will complement current research on the diversity and ecology of bat species at various elevations throughout Panama. 9

STUDY AREA

Shared equally between Panama and Costa Rica since 1988, La Amistad, or the Friendship International Park comprises an area of approximately 207 ,000-ha in

Panama alone, second only to The Darien National Park in size, and contains seven of

Holdridge's 12 life zones (Acosta 1991). In Panama, La Amistad is located in the nation's two most westerly provinces, Bocas del Toro (97%) and Chiriqui (3%), the latter of which offers the only entrance to the park accessible by road (Acosta 1991 ).

Declared a World Heritage Site by UNESCO in 1990, La Amistad forms a part of the

La Amistad Biosphere Reserve and the Meso-American Biological Corridor

(A.N.A.M. 1998). Despite its size and notoriety, limited information exists on the diversity and ecology of plants and animals living within the park.

This research took place in the primary and secondary cloud forests surrounding the ranger station in La Amistad International Park, located in the community of Las Nubes, Province of Chiriqui, Republic of Panama (Figure 1). Once clear-cut for use as a dairy farm, an 80-ha area of approximately 13-year old forest immediately surrounds the ranger station, in which A/nus spp. and Marvaceae spp. are abundant (M. Osawa, unpublished data). Mature cloud forest extends out from this regeneration area and is dominated by Quercus spp. (M. Osawa, unpublished data).

Vegetation in the disturbed landscape is fairly homogenous and open, dominated by young trees with a canopy height of approximately 25 m and a less dense understory, relative to the primary forest. Vegetative structure in the IO

,.. ,..,.. __ .... El Retofio. trail ,., • .. t I • . t• • ', La Montana trail Road to ... Las Nubes (~1 km)

035km • Parque Internacional La Amistad, Las Nubes, Chiriqui Ranger station • Primary forest sites· ■ Secondary forest sites

Figure 1. Map of study area, Parque Internacional La Arnistad, located in Las Nubes, Province of Chiriqui, Republic of Panama. 11

undisturbed forest is more complex, characterized by old trees with high canopies

(approximately 35 m), which serve as habitat for a diverse array of plants, including bromeliads, orchids, and liana, and a denser understory. The landscape is, however, less homogenous than the disturbed area, due to frequent tree falls, which form natural gaps in the forest and are largely a result of strong northerly winds.

Elevation in the study area ranges between 2200 m and 2500 m (A.N.A.M.

19,98) and clouds and mist are present for much of the day. Rainfall averages 3900 mm per year with a drier season occurring in the months of February and March

(A.N.A.M. 1998). Daily temperatures fluctuate between a mean minimum of 10° C and a mean maximum of22° C (A.N.A.M. 1998, Appendix 1). 12

· METHODS

Mist Net Sampling

Bats were netted in two habitat types, primary and secondary cloud forest.

Three sites in each forest type were sampled, which were located along existing trails

(El Retofio and Vereda La Montana) at intervals of approximately 500 m. Within each site, three permanent netting stations were constructed at least 100 m apart, depending on the terrain, and, where possible, were chosen to sample the following microhabitats: forest flyway (e.g., trails), water (e.g., stream), and forest gap (Figure

1). Following Bonaccorso's (1979) methodology and Kunz and Kurta's (1988) guidelines for net set-up using ropes and pulleys, each netting station contained a set of parallel mist nets (38 mm mesh; 12 m x 2.5 m), with one net placed in the understory (0-3 m) and one hung in the subcanopy/canopy (8-15 m), hereafter referred to as the canopy.

Despite their well-known bias in under-representing more adept flyers, such as the aerial insectivores, mist nets were chosen for their overall ease of use, effectiveness in catching most phyllostomid species, which predominate in the tropics, and because they allowed for the collection of valuable information on reproductive state and sex ratio. To get a more accurate picture of the composition of the phyllostomid community in the cloud forests of La Amistad, understory and canopy levels were netted simultaneously.

Each of the six sites was netted for two consecutive nights (1800-2400 hr) or one all-night sampling session (1800-0600 hr) during the last and first quarter of the moon of each month over the 6-month study period (Morrison 1978). If it began 13 raining during the sampling night, all six nets of the site were closed until it stopped raining, when all were reopened and sampling continued. In the case of continuous and substantial rainfall (~3 hrs), sampling resumed the following night, so that all sites received comparable monthly sampling efforts (approximately 12 hrs/ month).

All nets were monitored for bats at least once every hour.

Once removed from the net, each bat was placed in a cloth bag until the following data were collected (no more than 1 hr after capture): species identification

(C.O. Handley Jr., Smithsonian, unpublished key for highland bats of Panama, Reid

1997), hour and location of capture (net station and vegetative strata), sex, relative age (adult or subadult), reproductive state of females, weight (g), and forearm length

(mm). Relative age was determined by transillumination of the wing. Subadults were identified by the presence of unfused metacarpal epiphyses (Anthony 1988).

Reproductive state was determined by gently palpating the abdomen for embryo presence (note: this technique only detects advanced stages of pregnancy) and by expressing the teats for milk (Racey 1988). Bats were marked using a plastic necklace fit with a numbered aluminum band and released at site of capture.

Data Analysis

Bat diversity, species richness, and abundance: Sampling effort was calculated as mist net hours (mnh), where one mnh equals one 12 m net open for one hour. Species diversity (H') was calculated for the La Amistad bat community as a whole, as well as in each forest type individually, by using the Shannon-Wiener Diversity Index, H' = - t Pi loge p1 (Krebs 1999). Likewise, species evenness (J') was estimated as J' = H' /

In S, where S was the number of species (Krebs 1999). Betweeri-forest diversity and 14 evenness indices were compared using paired t-tests at alpha level 0.05 (Zar 1996).

The following variables also were calculated at both the community and habitat levels: species richness (S, total number of species registered), relative abundance (% of total individuals of a given species captured during a defined period of time) and monthly capture rates (number of captures of a given species per month per 100 mist net hour).

Vertical Stratification: Preference for canopy versus understory strata was analyzed by comparing the total number of captures per species in each strata with a Chi­

Square Goodness of Fit test at alpha level 0.05 (Zar 1996). This tested the assumption that if bats were using the strata without preference, a 1 : 1 ratio of presence in canopy to understory nets would be expected.

Nightly Activity Patterns: To observe temporal patterns in flight activity throughout the night for the study period, frequency of capture was calculated for each of the five most common species during six two-hour time periods, beginning at zero hours after sunset (1800 hr) and ending at 12 hours after sunset (0600 hr). Frequency of capture was determined by calculating the total number of captures of each species in each of the six time periods for the study period and then converting this to a percentage based on the total number of captures for each species.

Feeding guild I body size niche matrix: Community structure in La Amistad was analyzed using a matrix of guilds originally proposed by McNab (1971) and adapted by Kalko et al. (1996) which assigns bat species to feeding guilds based on their habitat use, feeding mode, and diet. They divided habitat, or the main foraging area of a bat, into three categories: uncluttered space, background cluttered space, and 15 highly cluttered space. Uncluttered space was defined as the open space high above the canopy or ground. Background cluttered space included forest edge, forest gaps, trails, and space between the canopy and subcanopy layers of the forest. Highly cluttered space was characterized by foraging near the ground or water level or within the vegetation. Foraging mode, or the manner in which bats obtain their food, was classified as either aerial, for food caught while in flight (e.g., flying insects,) or gleaning, for food taken from surfaces (e.g., fruit, nectar, non-flying insects). Diet was the food taken most frequently by a particular bat species. Since my study did not examine food preference, diet information was based on the literature

(Bonaccorso 1979, Kalko et al. 1996) and local experts (R. Samudio Jr., Smithsonian

Tropical Research Institute, personal communication). Following suggestions by

LaVal and Fitch (1977), the niche matrix for the La Amistad bat community was constructed using mean weight (g) as an index of body size, since two species of similar forearm length may differ substantially in weight. The smaller bat would be expected to have a lower ecological impact due to its consumption of fewer resources than the larger bat (Lim and Engstrom 2001 ).

Reproductive Ecology: For each of the five most common bat species, sex ratio was calculated for the entire 6-month study period and by month by calculating the ratio of adult female to male individuals in the population sampled. Using a Chi-Square

Goodness of Fit test, monthly sex ratios were tested for deviance from the expected

1: 1 ratio at alpha level 0.05 (Zar 1996). 16

RESULTS

DIVERSITY, RICHNESS, AND ABUNDANCE OF LA AMISTAD BATS

Between June and November of 2001, I sampled 56 nights for a total effort of

2548 mist net hours (mnh). Monthly sampling effort had a mean value of 425 mnh and ranged from 390 (November) to 459 (July) mnh. The cumulative species curve for the La Amistad bat community tended to level off around 42 nights, suggesting a reasonably complete representation of the nettable species occurring during the study period, although rarer species may have gone undetected (Figure 2). Diversity and evenness for the entire La Amistad bat community across the entire study period were estimated at H' = 1.58 and J' = 0.58. Species diversity was greatest in June with H' =

1.63 and lowest in July and November with H' = 1.12. Species richness was the same for all months with nine species, except for November when seven species were present (Appendix 2). I captured a total of 1050 individuals (123 were recaptures for a total of 1173 captures) representing 15 species and two families, eight genera of

Phyllostomidae and two genera ofVerspertilionidae (Table 1). Of this total, 653 were frugivores (seven species), 368 were nectarivores (three species), and 29 were aerial

(four species) and foliage-gleaning (one species) insectivores.

Four frugivores and one nectarivore accounted for 98.6% of all frugivores and nectarivores captured. Anoura geoffroyi, the nectarivore, was the most abundant

species, accounting for 35.6% of all frugivores and nectarivores captured, followed by the frugivores Sturnira hondurensis (29.5%), Artibeus aztecus (23.3%), Sturnira

mordax (5.6%), and Artibeus toltecus (4.7%). These species represent the most

common phyllostomid species in La Amistad based on both their abundance and 17

II) 16 Cl) ·u 14 Cl) 0. ....u, 12 0 10 ..Cl) .c 8 E ::::, z 6 ~ 4 ~ca :i 2 E ::::, 0 0 1 4 7 10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55 Consecutive Net Nights

Figure 2. Cumulative number of bat species captured in the cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001. 18

Table 1. Number of captures of bat species in Parque Internacional La Amistad, Panama, during 56 sample nights between June and November 2001.

Scientific Name Family 8 Total Individuals No. nights captured {Total Ca~tures) Anoura geoffroyi p (G) 363 (398) 44 Sturnira hondurensis p (S) 301 (322) 51 Artibeus aztecus p (S) 238 (274) 38 Sturnira mordax p (S) 57 (88) 42 Artibeus toltecus p (S) 48 15 Myotis keaysi V 14 11 Myotis oxyotus V 6 5 Echisthenes hartii p (S) 5 5 Myotis nigricans V 5 4 Micronycteris microtis p (P) 3 3 Lichonycteris obscura p (G) 3 3 Glossophaga soricina p (G) 2 2 Artibeus lituratus p (S) 2 2 Platyrrhinus vittatus p (S) 2 2 Eptesicus brasiliensis V 1 1

TOTAL= 15 2 1050 (1173) 56 a P = Family Phyllostornidae with subfamilies: (P) Phyllostirninae, (G) Glossophaginae, and (S) Stenodermatinae; V = Family Vespertilionidae 19

presence throughout the study period (n ~ 5 months). One aerial insectivore, Myotis keaysi, was the most common insectivore species captured in La Amistad, representing roughly half of all insectivorous bats captured. The nine remaining bat species were found to be uncommon in La Amistad, based on their low sample size (n

::;; 6 individuals) and temporary presence (n::;; 3 months) (Appendix 3).

TEMPORAL DISTRIBUTION OF LA AMISTAD BATS

Monthly Activity Patterns

Monthly capture rates varied for the five most common bat species in La

Amistad over most of the wet season of 2001 (Figure 3). In July, Sturnira hondurensis was the most abundant species with a capture rate of 24.2 bats per 100 mist net hours (pbnh). A second peak in abundance was observed in October but to a lesser extent at 17 .8 pbnh. Abundance of its sympatric species Sturnira mordax displayed a similar bimodal pattern with peak capture rates occurring in July at 5.2 pbnh and again in October at 2.9 pbnh. A gradual increase in abundance of Anoura geoffroyi was recorded between July and October, at which time abundance reached its seasonal peak at 32.3 pbnh. The following month, in November, few individuals of A. geoffroyi were observed and Artibeus aztecus hit its seasonal peak at 32.3 pbnh.

As with A. aztecus, abundance in its sibling species, Artibeus toltecus, was found to similarly peak in November at 7.4 pbnh.

Nightly Activity Patterns

Frequency of capture through the night was used to measure overall patterns in flight activity for the five commonest species in La Amistad over the study period. 20

35

30 C: E 25 0 ...... 0 ,_ Q) a. U) ~ ::, ....a. (\l t) A. toltecus S. mordax S. hondurensis

Figure 3. Monthly capture rates for the five most common phyllostomid bat species in Parque Internacional La Amistad, Panama, from June to November 2001. 21

(a) Ill G) -+-A. geoffroyi ....!::i 50 iu 40 30 s0 20 =....0 C 10 G) u ..G) 0 ll. 0 2 4 6 8 10 12

(b) 40 -+-S. hondurensis _._s, mordax 30 -

20

10

0 2 4 6 8 10 12

(c)

50 -+-A. aztecus 40 - - A. toltecus 30 20 10 0 0 2 4 6 8 10 12 Hours after sunset

Figure 4. Frequency of capture through the night as a measure of flight activity for Anoura geoffroyi (n = 398) (a), Sturnira hondurensis (n = 322) and Sturnira mordax (n = 88) (b), and Artibeus aztecus (n = 274) and Artibeus toltecus (n = 48) (c) in Parque Internacional La Amistad, Panama, from June to November 2001. 22

Cl) -+-A. aztecus ·c;Cl) Cl) Q. 50 - S. hondurensis Cl) .c CJ 40 ----S. mordax ftl Cl) ...0 30 Ri 20 -0 ...-0 10 C -Cl) 0 ~ Cl) C. 0 2 4 6 8 10 12 Hours after sunset

Figure 5. Frequency of capture through the night as a measure of flight activity for A. aztecus (n = 80), S. hondurensis (n = 76), and S. mordax (n = 13) in Parque Internacional La Amistad, Panama, during October 2001. 23

Distinct unimodal patterns of flight activity were observed for each of the three genera, such that activity peaks occurred at different times of the night. Flight activity in Anoura geoffroyi, peaked earlier than species from the other two genera, with 46.5% of the total captures for this nectarivore occurring during the first hours after sunset (Figure 4a). In Sturnira species S. hondurensis and S. mordax, abundances peaked between two and four hours after sunset at 35.4% and 33% of total captures for each species, respectively (Figure 4b). Following this peak, activity in S. hondurensis immediately dropped off, decreasing gradually throughout the night.

S. mordax, on the other hand, sustained this high level of activity until about midnight, at which time activity declined rapidly. Flight activity for Artibeus species during the study period was greatest between four and six hours after sunset, when

30.7% of all A. aztecus captures and 39.6% of all A. toltecus captures were recorded

(Figure 4c). Unlike A. toltecus, however, A. aztecus displayed greater flight activity earlier in the night, which increased steadily until midnight and then began dropping off.

In October when capture rates increased simultaneously for the two most common frugivore species, A. aztecus and S. hondurensis, patterns in flight activity for these species did not differ markedly (Figure 5). Rather, both species maintained high levels of activity throughout the night, suggesting that fruits were abundant and

interspecific competition for these resources was minimal. Activity in S. mordax remained greatest between two to four hours after sunset, dropping off thereafter. 24

SPATIAL DISTRIBUTION OF LA AMISTAD BATS

Primary vs. Secondary Cloud Forest

Sampling effort between disturbed and undisturbed cloud forests was approximately equal for the study period. Neither species diversity indices, H', (t =

0.687, df= 5,p = 0.523), nor evenness indices, J' (t = 1.127, df= 5,p = 0.311) were significantly different between forest types (Table 2, Appendix 4). Bat abundance, however, was substantially greater in second-growth forest than mature forest as evident when overall capture rates were compared between forest types. Capture rate in secondary forest (58.4 pbnh) was more than twice as great as that encountered in primary forest (23.6 pbnh). . Species lists for the two forest types contained considerable overlap, sharing 10 of the 15 species (Appendix 5). Two insectivorous species, Micronycteris microtis (n = 3 captures) and Eptesicus brasiliensis (n = 1) were encountered exclusively in mature forest. While one insectivore Myotis keaysi

(n = 14) and two large frugivores, Artibeus lituratus (n = 2), and Platyrrhinus vittatus

(n = 2), were captured only in secondary-growth habitat.

Five species accounted for 94.6% and 96.4% of all individuals captured in: primary (n = 282) and secondary (n = 752) cloud forests, respectively. In primary forest, A. aztecus was the most abundant species, accounting for 38.6% of total individuals, followed by A. geoffroyi (25.8%), S. hondurensis (18.8%), S. mordax

(7.7%), and A. toltecus (3.7%). While in secondary forest, A. geoffroyi was the most abundant species (38%), followed by S. hondurensis (32.6%), A. aztecus (16.4%), A. toltecus (4.9%), and S. mordax (4.5%). 25

Table 2. Bat species richness, abundance, mean species diversity (H'), and mean evenness (J') in the primary and secondary cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001.

Forest Type Total Net hours Species Individuals H' (St. Dev.)* J' (St. Dev.)* Primary 1261 12 298 1.31 (0.333) 0.71 (0.16) Secondary 1287 13 752 1.16 (0.325) 0.59 (0.14) * Mean diversity calculatedfrom six, monthly diversity indices for each forest type 26

Habitat preference by species was analyzed for all bat species with adequate sample size (n > 6) (Figure 6). While present in both forest types, A. geoffroyi, S. hondurensis, and A. toltecus were significantly more abundant in secondary forest, suggesting they preferred this habitat. Aerial insectivore, Myotis keaysi, was found to prefer secondary forest as well and no individuals were captured in primary forest. A. aztecus and S. mordax did not appear to be selecting for one forest type over another as evident by their near equal occurrence in both disturbed and undisturbed forest sites.

Vertical Stratification

Sampling effort was approximately equal between vegetative strata for La

Amistad cloud forest. At ground level, 257 individuals of 11 species (both families) were caught in 1285 mnh, while in the canopy, 916 individuals of all 15 species were caught in 1263 mnh (Table 3).

Capture rate differed markedly between the two vegetative layers, with a value of 20 pbnh in the understory compared to 73 pbnh in the canopy. Approximately 78% of all captures (n = 1173) were taken from the canopy nets. Four of the five common species, A. geoffroyi, S. hondurensis, A. aztecus, and A. toltecus, were found significantly more in the upper levels of the forest, although all used the understory level (Table 3). In contrast, S. mordax was encountered almost equally in ground and canopy nets. Myotis keaysi, on the other hand, was captured significantly more at groundstory level. Low sample size (n ~ 3) for six of the 15 species prevented meaningful analysis of stratum preference by these species. However, for all but one,

Glossophaga soricina, there appeared to be a tendency for greater canopy use. 27

30

308"" 25 □ Primary .c: C: 20 .Q C.

1/) Ill Secondary - 15 ~ ::, -C. ffl (.) 10

5

0 +---'---- A. geoffroyi A. aztecus S. hondurensis S. mordax A. toltecus

Figure 6. Capture rate (captures/pbnh) for five most common bat species in primary and secondary cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001 (**=significantly different at p < 0.01). 28

Table 3. Vertical stratification by bats captured in cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001.

CAPTURES Species Understory Canopy Total (0-3m) (8-15m) Anoura geoffroyi 58 340** 398 Sturnira hondurensis 109 213** 322 Artibeus aztecus 23 251** 274 Sturnira mordax 43 45 88 Artibeus toltecus 4 44** 48 Myotis keaysi 11 * 3 14 Myotis oxyotus 4 2 6 Echisthenes hartii 1 4 5 Myotis nigricans 1 4 5 Micronycteris microtis 2 1 3 Lichonycteris obscura 0 3 3 Glossophaga soricina 1 1 2 Artibeus lituratus 0 2 2 Platyrrhinus vittatus 0 2 2 Eptesicus brasiliensis 0 1 1

Total 257 916 1173

* Significantly different at p < 0. 05 ** Significantly different at p < 0. OJ 29

Preference for vegetative strata was consistent between forest types, e.g., species did not significantly change their preference for forest layers, whether captured in primary or secondary forest (Appendix 6). 30

COMPOSITION AND STRUCTURE OF LA AMISTAD BAT COMMUNITY

Feeding Guild / Body Mass Niche Matrix

Each of the 15 bat species observed in La Amistad during the wet season of

2001 was assigned to one of the ten feeding guilds delineated by Kalko et al. (1996) based on their habitat use, feeding mode, and diet (Table 4). Each species was placed into weight categories based on mean adult body weight (g), since sexual size dimorphism was weak in most species and did not prevent males and females from occupying the same niche matrix cell (Appendix 7). Only five of the ten feeding guilds were represented by the 15 bat species registered in the La Amistad between

June and November 2001 (Table 5).

Highly cluttered space/gleaning frugivore was the richest guild both in terms of species richness (n = 7) and distribution across weight classes (n = 4). Of the two species found to occupy the small size class, only one, Artibeus toltecus, was encountered frequently in La Amistad, while Echisthenes hartii was captured occasionally during the study period. Three of the commonest frugivore species for

La Amistad, Sturnira hondurensis, Sturnira mordax, and Artibeus aztecus, shared the medium size category. Of the two congeneric species, S. hondurensis was numerically dominant to S. mordax, as evident from monthly capture rates (Figure 3).

The average mass of these sibling species also differed by at least 6g. The large and very large frugivore size classes were occupied by one species each, Platyrrhinus vittatus and Artibeus lituratus, respectively. Both species were caught only twice towards the end of the wet season. 31

Table 4. Guild designations, mean weights (g), and mean forearm lengths (mm) for bat species captured in Parque Internacional La Amistad, Panama, between June and November 2001.

Species Mean Weight (g) Mean Forearm ±St.Dev. a Length (mm) ±St.Deva Anoura geoffroyi N /2 15.5 ± 1.4 42.6 ± 1.2

Sturnira hondurensis FI 2 21.6 ± 2.3 44.1 ± 1.3 Artibeus aztecus FI 2 24.8 ± 2 47.9 ± 1.6 Sturnira mordax FI 2 27.5 ± 3.2 46.8 ± 2 Artibeus toltecus FI 2 16.3 ± 1.8 41.3 ± 1.6 Myotis keaysi AI/ l 5.7 ± 1.3 36.4 ± 1.7 Myotis oxyotus AI/ 1 8 ± 0 41 ± 0 Echisthenes hartii FI 2 19.4 ± 2.1 38 ± 5.7 Myotis nigricans AI/ 2 5 ± 0.8 36.8 ± 0.5 Micronycteris microtis FGI / 1 9 ± 0 35 ± 0 Lichonycteris obscura N I 2 7 ± 0 31 ± 0 Glossophaga soricina NI 2 9.5 ± 3.5 36.5 ± 3.5 Artibeus lituratus FI 2 71.5 ± 3.5 69 ± 0 Platyrrhinus vittatus FI 2 56.5 ± 0.7 59.5 ± 0.7 Eptesicus brasiliensis AI / 3 6 ± 0 b 40 ± 0 b a All weights and lengths based on adult measurements, unless otherwise stated b Weight and forearm length taken from one male subadult c Feeding Guilds: N, nectarivore; F, frugivore; FGI, foliage-gleaning insectivore; AI, aerial insectivore; 1, background cluttered space; 2, highly cluttered space; 3, uncluttered space Table 5. Niche matrix for La Amistad bat community, based on 15 species of bats captured in cloud forests of Parque Internacional La Amistad, Panama, between June and November of 2001.

Guilds Mean Weight (g) Space / feeding mode Very small Small Medium Large Very large TOTALS ~10 11-20 21-40 41-60 61-90 Uncluttered space/ aerial insectivore 1 (a) 1 Background cluttered space/ aerial insectivore 3 (bed) 3 Highly cluttered space/ aerial insectivore 0 Highly cluttered space/ gleaning insectivore 1 (e) 1 Highly cluttered space/ gleaning carnivore 0 Highly cluttered space/ gleaning piscivore 0 Highly cluttered space/ gleaning sanguivore 0 w Highly cluttered space/ gleaning frugivore 2 (fg) 3 (hij) 1 (k) 1 (1) 7 N Highly cluttered space/ gleaning nectarivore 2 (mn) 1 (o) 3 Highly cluttered space/ gleaning omnivore 0

TOTALS 7 3 3 1 1 15 Cells occupied 4 2 1 1 1 9 Species: a, Eptesicus brasiliensis; b, Myotis keaysi; c, Myotis oxyotus; d, Myotis nigricans; e, Micronycteris microtis; f, Artibeus toltecus; g, Echisthenes hartii; h, Sturnira hondurensis; i, Artibeus aztecus; j, Sturnira mordax; k, Platyrrhinus vittatus; I, Artibeus lituratus; m, Lichonycteris obscura; n, Glossophaga soricina; o, Anoura geoffroyi 33

Similar to the nectarivores, the background cluttered space/aerial insectivores composed the next richest guild with three species. All three species occupied the t very small size class and were from the same genus. Two species, Myotis keaysi and

Myotis nigricans were of similar weight, while Myotis oxyotus was larger than the other two, both in body mass and forearm length. M keaysi was the only species commonly encountered throughout the study period, while the other two were captured infrequently.

Nectarivores occupied two size classes and all three were from different genera. Two species, Glossophaga soricina and Lichonycteris obscura, occupied opposite ends of the very small size category, with the former at the higher limit for mean body mass. Both were found to be uncommon in La Amistad during the study period. Anoura geojfroyi was the only small-sized species and was the dominant phyllostomid species in La Amistad during the wet season of 2001.

The two remaining guilds (uncluttered space/aerial insectivore and highly cluttered space/gleaning insectivore) were occupied by only one species each. Both the aerial insectivore Eptesicus brasiliensis and the foliage gleaning insectivore

Micronycteris microtis were found to be uncommon and present only in primary cloud forest.

Overall for the feeding guild and body mass niche matrix, only nine of the 50 possible cells were filled. Of these nine, four cells were occupied by more than one species. Of these four, three were composed of species from different genera. The two most represented cells were the small background cluttered space/aerial 34 insectivores and medium-sized highly cluttered space/gleaning frugivores, with three species each.

REPRODUCTIVE ECOLOGY OF LA AMISTAD BATS

Due to small sample size (n ~ 6) in many of the less common bat species (n =

7), reproductive activity of adult females captured during the wet season of 2001 could not be assessed (Appendix 8). Reproductive state of adult females was compared among the five most common bat species. They displayed considerable variation among species. No reproductively active (palpably pregnant or lactating) adult females were detected for A. aztecus (n = 130) from June to November 2001.

For A. toltecus, there was an absence of adult females captured from June through

September, at which time nine individuals were captured (October). Of these, 33% were detectably pregnant (n = 1) or lactating (n = 2). In November, all adult females

(n = 27) were observed to be in a non-reproductive state. Twenty-seven percent of

109 adult female A. geojfroyi were in advanced stages of pregnancy or were lactating during the study period. Palpably pregnant females of this species were observed from August to October and one lactating individual was observed in June (Figure

7a). Twenty-nine percent of 128 adult females of S. hondurensis were reproductively active in all months except August (no adult female captures) and November (Figure

7b). S. mordax had the highest percentage of reproductively active females with 54% of 48 individuals detectably pregnant or lactating. Lactating individuals of this species were observed in all months but October and only one pregnant female was detected in August (Figure 7c). 35

(a)A. geoffroyi (n = 109) II Pregnant u, a, ii 100 ■ Lactating E 80 .! 24 :i- 60 "CJ C'CI .... 40 45 0 C 20 11 17 -a, 11 1 mm ~ I a, 0 I I D. • J J A s 0 N

(b)S. hondurensis (n = 128)

100 80 19 60 8 40 20 9 11 0 J J A s 0 N

(c)S. mordax (n = 48)

1ijlir~--~-5~-~--j~~-8-~~--6~ J J A s 0 N Month

Figure 7. Reproductive condition of adult female A. geojfroyi (a), S. hondurensis (b ), and S. mordax ( c) captured by month in Parque Internacional La Amistad, Panama, between June and November 2001. 36

Table 6. Sex and age distribution among bat species captured in cloud forests of Parque Internacional La Amistad, Panama, from June to November 2001.

Species Adult Individuals Subadult Individuals Total {#F /#M) {#F /#M) Individuals Anoura geoffroyi 104 / l 79** 47 I 33 363 Sturnira hondurensis 116/64** 78 / 43** 301 Artibeus aztecus 127 / 104 2/5 238 Sturnira mordax 34 I 16* 5/2 57 Artibeus toltecus 36 I 9** 2/1 48 Myotis keaysi 6/1 5/2 14 Myotis oxyotus 2/0 4/0 6 Echisthenes hartii 3/2 0/0 5 Myotis nigricans 1/3 1/0 5 Micronycteris microtis 1 /1 1/0 3 Lichonycteris obscura 0/1 1 /1 3 Glossophaga soricina 1 / 1 0/0 2 Artibeus lituratus 1 /1 0/0 2 Platyrrhinus vittatus 0/2 0/0 2 Eptesicus brasiliensis 0/0 0/1 1

Total 816 (432 / 384) 234 {146 / 88)** 1050 * significantly different from 1: 1 at p < 0.. 05 * * significantly different from 1: 1 at p < 0.01 37

Few subadults of A. aztecus (seven out of 238 individuals) and A. toltecus

(three out of 48 individuals) were observed during the study period (Table 6). The highest percentage of subadults captured was by S. hondurensis, with 40% of the 301 individuals captured. Subadults of this species were captured throughout the study period, with 80% of the 124 subadults being observed in July and August (Figure 8b).

Ten percent of the 80 S. mordax captured were subadults and observed only in July and August (Figure 8c ). In the highly abundant nectarivore A. geoffroyi, subadults comprised only 22% of the 363 individuals captured, most of which (86.6%) were caught in August and September (Figure 8a).

Overall for the study period, the ratio of adult males (n = 384) to adult females

(n = 432) did not differ significantly from 1: 1 (X2 = 2.824, df = 1; p = 0.09) (Table 6).

However, monthly comparisons revealed that a significant female bias existed during

June (X2 = 4.945, df = 1; p = 0.03), July (X2 = 16.011, df = 1; p < 0.001), and

November (X2 = 13.880, df = 1; p < 0.001) and a significant male bias was evident in

August (X2 = 5.444, df = 1; p = 0.02). Overall female-biased sex ratios were found for S. hondurensis (X2 = 19.814, df= l;p < 0.001), S. mordax (X2 = 8.000, df= l;p =

0.01 ), and A. toltecus (X2 = 16.200, df = 1; p < 0.001 ), while a male-biased sex ratio was observed in A. geoffroyi (X2 = 24.164, df = 1; p < 0.001 ). Sex ratio in A. aztecus was not shown to differ significantly from 1: 1 for the study period (X2 = 0.254, df = 1; p = 0.614).

As was the case in the total overall sex ratio, sex ratios for the most common bat species demonstrated heterogeneity across months (Figure 9). Males of A. geoffroyi were most abundant in only four of the six months, while female adults of S. 38

(a) A. geoffroyi ■ Adults 19 136 ■ Subadults 100 31 U) 15 -a; 80 68 ::, 112 "O 60 ·s; '6 40 .5 20 0~ 0 J J A s 0 N

(b) S. hondurensis 10 75 100 32 21 80 60 60 40 20 0 J J A S O N

(c) S. mordax 15 8 12 6

1:: 1ti 15 ~l

J J A S O N Month

Figure 8. Percentage of adult and subadult individuals of A. geoffroyi (a), S. hondurensis (b ), and S. mordax ( c) captured in Parque Internacional La Amistad, Panama, between June and November 2001. 39

A. geojJroyi "" i " II.Ii " 's :¥ ,. ;/1,

=25' ::.ii ,., j" "'100

S. hondurensis

75

A. aztecus

25 ,.

100

S. mordax

"

25 "'

15 Months

Figure 9. Sex distribution for common phyllostomid species in Parque Internacional La Amistad, Panama, between June and November 2001. (*=significantly different at p < 0.05; **=significantly different at p < 0.01) 40 hondurensis and A. toltecus were significantly more abundant than their male counterparts in June and July for the first species and November for the latter one.

Sex ratio in A. aztecus and S. mordax did not differ significantly from 1: 1 across months, except for the month of July when more males of A. aztecus were caught. 41

DISCUSSION

TEMPORAL DISTRIBUTION OF LA AMISTAD BATS

As elevational patterns elsewhere in the tropics might predict, bat diversity in highland regions, such as La Amistad (2300 m), appears to be lower than that found in the lowlands of Panama. The Shannon-Wiener diversity index for the La Amistad bat community was estimated to be 1.58 during the wet season of 2001 (June to

November). This value is similar to the value of 1.62 recorded by Soriano (1983) for bat diversity in the cloud forests of Monte Zerpa (2100 m) in Venezuela. In two lowland forests, Cristobal (5 m) and Balboa (50 m) in the former Panama Canal Zone,

Fleming et al. (1972) recorded bat diversity as 1.98 and 1.89, respectively.

Species richness was also greater in these lowland sites than in La Amistad.

Thirty-one species comprised the bat fauna of Cristobal, while in Balboa 27 bat species were recorded. While these sites contained many more species than La

Amistad, more intensive sampling protocols through the use of canopy nets in addition to the understory nets employed may have revealed even greater species richness, especially by canopy frugivores and nectarivores. It is highly probable that the composition of the La Amistad bat community, with its first approximation of richness at 15 species, may be underrepresented as well since sampling was conducted during only the wet season and because the sampling protocol may have failed to detect many insectivorous species. Aerial insectivores are especially difficult to capture via mist netting due to their high-flying foraging behavior (above canopy) and acute ability to assess their surroundings via echolocation (Kalko et al. 1996). On

Barro Colorado Island in the Panama Canal, a long history of intense mist netting and 42 trapping at canopy and understory levels, in addition to acoustic monitoring, has lead to the identification of at least 66 species of bat, representing eight families, using these forests.

Recently, a 3-year dissertation study comparing the bat community found in a mid-elevation cloud forest (1200 m) with that of a lowland site (135 m) was concluded in Western Panama (R. Samudio Jr., University of Florida, Gainesville/

Smithsonian Tropical Research Institute, personal communication). Both communities had similar species richness (34 and 35 species, respectively), however the cloud forest community had a much greater diversity index (2. 7) than the lowland community (2.17). These results suggest that more intense sampling at both middle and high elevations is needed to better understand the relationship between bat diversity and elevation.

Monthly bat diversity values for La Amistad ranged from a low of 1.12 in both

July and November to a high of 1.63 in June (Appendix 2), reflecting fluctuations in species composition throughout the wet season. Species composition describes both the number and the types of species present in a community (McNab 1971). In La

Amistad, the number of bat species remained relatively constant throughout the study period with nine species, except for the month of November when only seven species were registered. The absence of aerial insectivores in November coupled with reductions in populations of the two dominant species for the wet season, A. geoffroyi and S. hondurensis, suggests that this might represent a time of low food abundance.

Reductions in fruit production have been reported to occur at the. end of the wet season and early in the dry season in both Panama and Costa Rica (Fleming et al. 43

1972, Bonaccorso 1979, Bonaccorso and Humphrey 1984, Dinerstein 1986). Insect abundance also has been reported to decline substantially during the Central

American dry season, when flower availability is greatest (Janzen 1967).

Disappearance of the common nectarivore A. geoffroyi from the study area might signal a depletion of local flower reserves (e.g., flowers of the Majaguillo tree,

Heliocarpus popayanensis) as individuals search for additional nectar sources in nearby regions.

The kinds of species comprising the La Amistad bat community and their relative abundances varied greatly by month. Approximately half of all species identified in La Amistad were present three months or fewer (Appendix 3). Each of these nine species was also found to be uncommon due to their infrequent capture history (n ~ 6 individuals) in La Amistad over the study period. The brevity of their stays paralleled by their relatively low abundances in this highland community suggest that these species reside elsewhere (other regions or elevations) but may visit the cloud forests of La Amistad when preferred food sources are temporally abundant.

Artibeus lituratus is one such species. A. lituratus is a common member of lowland faunas, but has been found to visit highland regions during certain times of the year

(Timm and La Val 2000, this study). Altitudinal migration by individuals of this species is likely a mechanism to improve individual fitness by taking advantage of asynchronous bursts in fruit production by abundant and widespread Ficus tree species. Further research is needed to determine whether the presence / absence of these uncommon bat species observed in La Amistad during the wet season coincides with fluctuations in food availability. 44

Five phyllostomid species, accounting for nearly 99% of all frugivores and nectarivores captured, represent the dominant species of the La Amistad bat community during the wet season. Their ability to exploit temporally available food resources is evident by changes in species abundance occurring at various times throughout the wet season.

In the sibling species Sturnira hondurensis and Sturnira mordax, capture rates hit distinct peaks twice during the study period, once in July and again in October.

Just before and during these peaks, large numbers of lactating females were captured

in La Amistad. A similar observation was documented in the premontane cloud

forests of Monteverde, where lactating females of S. hondurensis were observed at the

beginning of the wet season (April-June) and again towards the end of the wet season

(September-October) and their occurrence coincided with peaks in Solanum fruit

biomass (Dinerstein 1986). The prevalence of lactating females in the La Amistad

community at these two points during the wet season suggests that S. hondurensis and

S. mordax may be cuing into periods of high fruit abundance, thereby timing their

energy-demanding reproductive events to take place at these same times. While both

species underwent synchronous peaks in abundance, it is clear that S. hondurensis is

the more abundant of the genus Sturnira in La Amistad. The larger resident

population of S. hondurensis suggests that this species might be better able to deal

with the constant cool temperatures and compete against S. mordax for access to

limited resources, primarily food and roosts.

As captures of S. hondurensis and S. mordax decreased following the first

peak in July, the nectarivore Anoura geo.ffroyi rose in abundance reaching its seasonal 45 peak in the month of October. This peak occurred at a time when the large, pale yellow flowers of the Majaguillo tree (Heliocarpus popayanensis) were plentiful, providing a rich source of nectar and pollen. This tree, found mostly in the secondary cloud forest of La Amistad, was observed to be in bloom between August and

October. During these months, mist nets coincidentally located near these flowering trees captured huge quantities of A. geoffroyi (65 captures in one October night), especially palpably pregnant females. As with the Sturnira species, reproduction in

Anoura geoffroyi appeared to coincide with periods of high food abundance (see also section on Reproductive Ecology). After this time, flowers fell to the ground and the presence of individuals of A. geoffroyi at the netting sites became greatly reduced.

At the beginning of the wet season, very few individuals of sympatric species

Artibeus aztecus and Artibeus toltecus were captured. While A. aztecus abundance increased gradually in subsequent months, only one A. toltecus individual was captured per month from June to September. Then in October, as S. hondurensis and

S. mordax were hitting their second peak in abundance, populations of A. aztecus and

A. toltecus began to increase markedly. Artibeus species are known to feed heavily on the fruits of Ficus plants (Bonaccorso 1979) and it is possible that local fig production may be greatest towards the end of the wet season at this elevation. The fact that representation by both genera was increasing proportionately in the community at the same time suggests that they were each tracking increases in food abundance. The greater number of A. aztecus than A. toltecus in La Amistad suggests that some level of interspecific competition, whether for food or roosts, might be occurring among these congeners, which allows A. aztecus to be more abundant at this elevation. In 46

Monteverde (1400-1600 m), on the other hand, A. toltecus was the most common

Artibeus species (Dinerstein 1986). This suggests that the ability of A. toltecus to successfully occupy forests at higher elevations depends on the presence of sibling species, such as A. aztecus, which may be more specialized to deal with the biotic and abiotic conditions of the region.

To determine whether these five species are in fact year-round residents of La

Amistad, additional fieldwork is required to document their presence both in the wet and dry season. Abundance trends among species are most likely influenced by the availability of abundant preferred· food sources, which are timed with energetically costly events, such as reproduction. Absence of a particular species for a substantial amount of the season (or year), such as was the case with A. toltecus, suggests that this species may be tracking food sources located elsewhere.

Consistent capture of Myotis keaysi throughout most the study period suggests that this aerial insectivore is also a resident of La Amistad, at least during the wet season. The relatively higher occurrence of M keaysi in the cloud forests of La

Amistad when compared to other aerial insectivores, however, may actually be due to its tendency to fly low along trails or clearings (Reid 1997) and thus, may not be as adept in detecting and avoiding mist nets. To better improve detection of insectivorous species in La Amistad, acoustic monitoring via bat detectors should be employed. Tracking these species across months will help to confirm whether M keaysi is indeed the most common insectivore in the community or whether it is just more susceptible to capture. 47

SPATIAL DISTRIBUTION OF LA AMISTAD BATS

Overall, bat diversity did not differ significantly between primary and secondary cloud forest in La Amistad and species richness was also similar. Evenness estimates did not differ significantly between disturbed and undisturbed forests and revealed that bat faunas in both forest types consisted primarily of a few common species, although other less abundant species were also present. Both species diversity and richness varied by month in the two forest types (Appendix 4). Likely, species are discriminating between the two forest types based on their food availability at that point in time. The substantial difference between abundance values for mature and secondary forest reveals the substantial use of disturbed habitat by 13 of the 15 species registered and especially by the five common species, which account for the majority of these captures.

The high degree of similarity in species composition between these two forest types suggests that the highland bat fauna of La Amistad may be composed of species with considerable flexibility in adapting to local disturbance events. The high energetic demands associated with residence in a constantly cool environment with limited resources (food and roosts) may select for those highland bat species with a more generalist strategy, whereby alternative food types are consumed when preferred food sources are low and existence is possible in habitats other than mature, undisturbed forest (Fleming 1986b, Estrada et al. 1993).

Of the 15 bat species detected in La Amistad, five were encountered exclusively in one forest type or the other. Primary forest contained two insectivorous species not shared by secondary forest, Micronycteris microtis and Eptesicus 48

brasiliensis. A member of the Phyllostominae subfamily, Micronycteris microtis is

considered a deep forest inhabitant whose foraging habits involve gleaning surfaces

such as logs and leaves for large insects and occasionally for fruit (Emmons 1997).

Perhaps one explanation for the presence of M microtis in primary forest rather than ·

secondary forest is the denser understory layer, which may provide greater cover and a

moister microhabitat for large insects. Phyllostomine bats have received attention for

their tendency to be found predominantly in undisturbed, primary forested habitats,

thereby acting as indicators of ecosystem integrity (Fenton et al. 1992, Wilson et al.

1992, Medellin et al. 2000). Perhaps the absence of M microtis from secondary

cloud forest habitat emphasizes just how recently the last major disturbance event

occurred in La Amistad (approximately 13 years ago) and how research is essential to

· understanding the habitat requirements of this species, as well as others that may also

be habitat specialists. In the case of E. brasiliensis, small sample size, due to a

sampling protocol that failed to detect many aerial insectivores, precludes inferences

about the habitat requirements of this species. According to Reid (1997), however,

this species commonly is associated with evergreen.forest and forest edge habitats, the

latter suggesting that some level of disturbance may be tolerated by this species.

On the other hand, one insectivore, Myotis keaysi, and two large frugivores,

Artibeus lituratus and Platyrrhinus vittatus, only occurred in secondary growth

habitat. Known to catch prey on the wing, M keaysi frequently forages in open areas

or gaps in the forest, such as along trails (Kalko et al. 1996). Perhaps this species'

preference for the disturbed habitat is a behavioral adaptation to enhance foraging

efficiency by hunting in the more open understory of the secondary growth forest, 49 containing less of the clutter which might interfere with echolocation. As one of the commonest species of fruit bat, A. lituratus is found at both high and low elevations

(Reid 1997) and this fact alone may imply an ability to adapt rapidly to local conditions. It is likely that this species, along with P. vittatus, uses both forest types, especially since this bat is known to take large canopy fruits, which in La Amistad may be available only in the mature forest. More information is needed to determine the degree (abundance and permanence) to which these species use the primary and secondary forests in La Amistad.

The high degree of similarity in species composition existing between the two forest habitats may be explained by the prevalence of the same five bat species:

Anoura geojfroyi, Sturnira hondurensis, Artibeus aztecus, Sturnira mordax, and

Artibeus toltecus. While each of these species was present in both primary and secondary forests, habitat preferences might explain observed shifts in dominance rankings among habitats. Based on capture rates, A. geojfroyi, S. hondurensis, and A. toltecus were encountered significantly more in nets set in disturbed forest, while A. aztecus and S. mordax were equally abundant in both disturbed and undisturbed sites.

In secondary forest, A. geojfroyi was the most dominant species, followed by S. hondurensis, A. aztecus, A. toltecus, and lastly S. mordax. In primary forest, A. aztecus was the most common species, followed by A. geojfroyi, S. hondurensis, S. mordax, and A. toltecus. The change in the order of dominance by these common species is due largely to greater occurrence of A. geojfroyi and S. hondurensis in the secondary forest. It is likely that these movements were motivated by the greater abundance of preferred food types. For instance, large numbers of A. geojfroyi were 50 captured near blooming flowers of the Majaguillo tree found primarily in secondary growth habitat. Likewise, S. hondurensis has been found to commonly feed on the fruits of Solanum (Dinerstein 1986, Fleming 1986a, Hemandez-Conrique et al. 1997), an early succession shrub common to disturbed habitats (LaVal and Fitch 1977).

Furthermore, individuals of A. geoffroyi and S. hondurensis seemed to be preferring one forest type over the other, since most recaptured individuals were encountered in the same forest type where they had been marked originally, usually secondary forest.

Most individuals of S. mordax and A. aztecus also appeared to be loyal to one forest or the other, although one individual of S. mordax was captured nine times over the study period occurring in five of the six primary and secondary forest sites netted.

Within each habitat, bat species were consistent in their preference for particular vegetative strata, as determined by their abundance (measured in capture rate) in canopy and understory nets. Four species, A. geoffroyi, A. aztecus, S. hondurensis, and A. toltecus, were significantly more abundant in the canopy nets in both primary and secondary cloud forests. On the contrary, S. mordax was found to use the canopy and understory layers equally in both forest types. The unbiased presence of S. mordax both within and among habitats suggests that this species may be more of a generalist in its feeding and roosting requirements, perhaps to minimize competitive encounters with the other frugivore species, particularly S. hondurensis.

COMPOSITION AND STRUCTURE OF LA AMISTAD BAT COMMUNITY

Five of the ten feeding guilds outlined by Kalko et al. (1996) were represented in La Amistad over the study period. It is possible that species from those guilds not represented do, in fact, reside in these cloud forests, but were not detected due to 51

limitations of the sampling protocol or seasonal bias (e.g., no data collected in dry

season). The lack of representation of all ten guilds also might suggest that highland

regions such as La Amistad do not contain the diversity of food types and sizes

necessary to support a more trophically diverse bat fauna. In three of the five feeding

guilds, multiple species coexisted, possibly a result of their differences in body size

which likely enabled them to partition available food resources based on particle size

(Hutchinson 1959).

Uncluttered Space/ Aerial Insectivore

This guild is composed of bats that forage for flying insects in open space,

high above the canopy or ground (Kalko et al. 1996). In La Amistad, one adult male

of Eptesicus brasiliensis weighing 6g was captured in a canopy net set across a trail in

. primary forest just after sunset. It is highly probable that this species and others of

this guild were not detected due to their tendency to fly high above canopy nets in

uncluttered space. Due to low sample size, habitat preference for E. brasiliensis

cannot be determined. However, the literature suggests that this species may be able

to tolerate some level of disturbance due to its presence in forest edge habitat (Reid

1997) and its use of a variety of roosts, including buildings (Emmons 1997).

Background Cluttered Space / Aerial Insectivore

In this guild, bats catch small insects on the wing in open spaces within the

forest, in forest gaps, and along forest edge (Kalka et al. 1996). Three species (family

Vespertilionidae) of very small size were captured. Representing more than half of all

captures for this guild, Myotis keaysi was numerically dominant to sympatric species

Myotis nigricans and Myotis oxyotus. It also appeared to be a resident of La Amistad 52 for most of the wet season based on its consistent occurrence in all months but

November, and the presence of two lactating females in June. All three species were captured during the first half of the night, primarily within two hours of sunset.

In terms of mean body mass, M keaysi ( 6 g) was most similar to M nigricans

(5 g). M nigricans, however, appeared to be less common with five captures all within the month of June, near the start of the wet season when insect abundance might have been higher (Janzen 1967, Fleming et al. 1972). Differences in spatial distributions may allow these two similar-sized species to coexist at certain times of the year. For instance, in La Amistad, M keaysi occurred significantly more in the understory while M nigricans displayed a non-significant tendency for the canopy.

With regards to habitat preference in La Amistad, M keaysi used exclusively secondary cloud forest, flying along trails and creeks and in forest gaps. This preference for secondary forest was documented in the cloud forests of Monteverde as well (LaVal and Fitch 1977). M nigricans, on the other hand, was captured in both primary (along creeks and in forest gap) and secondary forest (in forest gap).

With a mean body mass of 8 g, M o:xyotus is larger than its sibling species and this larger size may allow it to feed on bigger insects than those taken by M keaysi, especially during the months of July, August, and September when both species were found to coexist. Like M nigricans, M o:xyotus was captured in both primary (along trails and in forest gap) and secondary forest ( along trails) and showed a non­ significant tendency for the canopy level.

The presence of M oxyotus and M nigricans in La Amistad may be under­ represented due to the ability of aerial insectivores, in general, to avoid mist nets 53

(Kalko and Handley 2001). M keaysi, however, tends to fly lower in the forest which may lead to its relatively frequent capture in ground level nets (Reid 1997, this study).

Further sampling via acoustic monitoring is necessary to determine the spatio­ temporal distribution of bats of this guild throughout the year.

Highly Cluttered Space / Gleaning Insectivore

This guild includes those bats that forage by gleaning insects from surfaces, such as foliage, tree trunks, the ground and water (Kalko et al. 1996). One very small species from the subfamily Phyllostominae, Micronycteris microtis, was the only member of this guild to be detected during the study period. M microtis was represented by three individuals, all of which were captured in nets placed along trails and in a forest gap in primary forest only. Individuals were captured in July, August, and November and were active around midnight and before sunrise. Preference for vertical strata in the forest could not be determined due to low sample size for this species.

Highly Cluttered Space / Gleaning Frugivore

Members of this guild glean fruit from trees and shrubs (Kalko et al. 1996). In

La Amistad this was the most specious guild with seven species (family

Phyllostomidae ), varying in size from small to very large.

Two species were assigned to the small size class for this feeding guild,

Artibeus toltecus (16 g) and Echisthenes hartii (19 g). A. toltecus was one of the most common frugivores in La Amistad, especially during October and November. E. hartii was captured occasionally with five individuals recorded in July, September, and November. Both species occurred in disturbed and undisturbed cloud forests, 54 although A. toltecus was caught significantly more in nets placed in secondary growth habitat. Canopy preference was demonstrated by both species, although only A. toltecus was significantly encountered there. In primary cloud forest, A. toltecus was found exclusively in the canopy. According to Dinerstein (1986), this species may specialize on mature canopy fruits when they are abundant. Dietary analysis is necessary to determine whether these species are feeding on the same fruits. The fact that E. hartii was encountered occasionally during the study period and represented by only a few individuals suggests that this species is not diminishing the resource base substantially for A. toltecus. Nightly activity cycles may prevent competition as well, in as much as E. hartii tended to avoid periods when activity in A. toltecus was greatest, particularly around midnight.

The medium size class was shared between the three most common frugivore species occurring in La Amistad over the study period. Sturnira hondurensis,

Artibeus aztecus, and Sturnira mordax had mean body weights of 22, 25, and 28 grams, respectively. The way in which S. mordax and A. aztecus distribute themselves spatially in the forest suggests that they may be using those areas less important to the most abundant frugivore, S. hondurensis. Both S. hondurensis and A. aztecus were captured significantly more in the canopy. However, A. aztecus may have minimized competitive encounters with S. hondurensis by using both forest types equally, while S. hondurensis was found most often in secondary cloud forest.

Like A. aztecus, S. mordax was a habitat generalist, being captured equally in both forest types, and in both forest strata. By using both higher and lower levels of the 55 forest, S. mordax may take advantage of patchily available resources and thus reduce competition with its sibling species S. hondurensis.

Dietary differences might allow these three species to coexist despite limited fruit availability at higher elevations. Sturnira and Artibeus are two common genera of phyllostomid bats that appear to specialize on core plant taxa with year-round fruit production (Heithaus et al. 1975, Bonaccorso 1979, Dinerstein 1986, Hemandez­

Conrique 1997, Giannini 1999). According to Fleming (1986a), Sturnira species feed selectively on fruits of the highly nutritious but patchily available fruits of Piper and

Solanum in the understory, while Artibeus species feed primarily on the nutritionally poor but abundant canopy fruits of Ficus and Cecropia. Meanwhile, congeneric species might avoid competition by switching to the underutilized core plant taxon.

For instance, S. mordax might avoid competition with the more abundant S. hondurensis by reducing its intake of Solanum and feeding more on Piper fruits

(Fleming 1986a). The fact that S. mordax was found equally in both habitat types and forest strata in La Amistad suggests that this species might be acting as more of a generalist by taking advantage of patchily available food resources throughout the forest to avoid competitive interference with S. hondurensis. Also, the 6 g difference in mean body mass may minimize competition by allowing S. mordax to feed on larger fruits of the same plant genera as S. hondurensis.

Temporal partitioning of fruit resources also may reduce interspecific competition among these three common frugivores. The fact that S. hondurensis was as abundant (based on capture rate) as A. aztecus in La Amistad during the month of

October suggests that these species may have been responding to parallel increases in 56 the abundance of each of their core plant taxa. Nightly patterns of flight activity among species for the study period showed a lag in peak activity times occurring between S. hondurensis and A. aztecus such that the former was captured most frequently between 2000 and 2200 hours, while the latter was most active from 2200 to 2400 hours. Perhaps S. hondurensis became active earlier to compete with S. mordax for a limited number of Piper and Solanum fruits, despite the possible increased risk of predation. A. aztecus, on the other hand, might not have been under the same time constraints to become active earlier, since it likely fed on Ficus fruits, which are typically more abundant at night. Nightly activity by S. mordax was very similar to that of S. hondurensis, except for its tendency to remain highly active for an additional two hours following the peak, followed by a quick decline in flight activity in this species. Perhaps S. mordax needed more time to find patchy resources and fulfill its energy requirements due to S. hondurensis taking the most obvious and plentiful fruits for the night in secondary forest sites. Dietary information for these three species, especially S. hondurensis and S. mordax is needed to determine how they are able to coexist while fulfilling their energy demands, especially during costly reproductive events. Furthermore, information on the roosting requirements of these species is necessary since competition for a limited amount of suitable roosts (tree hollows and caves) may also affect their distribution and survival in the thermally challenging environment characteristic of the highlands of La Amistad.

Only one species of large frugivore, Platyrrhinus vittatus, was captured in La

Amistad during September and October. Two individuals were caught in canopy nets located in secondary cloud forest (trail and forest gap sites) during the first half of the 57 night. Based on its size, this species would be expected to feed on large fruits from tree species common to mature forest. The absence of P. vittatus in primary forest habitat suggests that the nets might not have been placed high enough to sample those individuals feeding in the canopy. Low abundance and occurrence of this species also suggest that the cloud forests of La Amistad might not produce enough large fruits to support a larger population of P. vittatus. More data need to be collected to determine the distribution of large fruits in La Amistad, as well as the degree to which this species uses these local fruiting sources throughout the year.

As with the large size class, the very large frugivore group was represented by one species, Artibeus lituratus, in the month of October. Two individuals of A. lituratus were encountered towards the middle of the night in secondary forest habitat

(trail and forest gap). Like P. vittatus, this species showed a non-significant tendency for the canopy layer, which has been documented previously (Bonaccorso 1979,

Bernard 2001, Kalko and Handley 2001). Common in the lowlands, A. lituratus specializes on large figs of the genus Ficus that grow in the forest canopy

(Bonaccorso 1979). Further studies may reveal that A. lituratus, and possibly P. vittatus migrate to higher elevations in Panama in search of temporarily available food sources, such as large figs (Timm and LaVal 2000).

Highly Cluttered Space / Gleaning Nectarivore

Nectarivorous bats forage from flowers of trees, shrubs, or vines, consuming primarily nectar and pollen and occasionally insects (Kalko et al. 1997). This guild contains three phyllostomid species, all from different genera, which are grouped into two size classes. 58

Two species, Lichonycteris obscura and Glossophaga soricina, represented the very small nectarivore size class. Both are primarily lowland species, typically encountered at elevations below 1000 m (Reid 1997) and were uncommon in La

Amistad, based on their low capture records. In June and August, three individuals of

L. obscura, one of which was dusted in yellow pollen, were captured during the first half of the night in canopy nets set across trails in both primary and secondary forest.

This species is considered one of the most rare species in the neotropics and little is known about its dietary and roosting habits (Arita 1993, Emmons 1997). In June and

October, two individuals of the larger species (by 3 g), G. soricina, were found in groundstory and canopy nets set across trails in both primary and secondary forest.

One individual was captured soon after sunset, while the other was captured just

before dawn. This species may eat both fruit (Kalko et al. 1996) and insects (Bernard

2001), especially in the wet season when flowers are less plentiful (Bonaccorso 1979).

Neither individual was dusted with pollen suggesting that they may have been

exploiting non-flower resources, even though Majaguillo flowers were abundant

during the month of October.

Anoura geoffroyi was the sole representative of the small nectarivore size

class and was also the most abundant phyllostomid species observed in La Amistad

during the study period. This species was observed frequently with yellow pollen

heavily dusted over the anterior portion of its body, especially during the months of

August, September, and October when flowers of the Majaguillo (Heliocarpus popayanensis) tree, common to the secondary cloud forest, were in bloom. Activity

patterns during these months revealed a consistent peak in activity during the first few 59 hours following sunset. A similar peak in activity early on in the night was recorded for several other species of nectar-feeding bat found to be important for the pollination of night-blooming plants, such as the Mexican columnar cacti (Valiente­

Banuet et al. 1996). It is likely that A. geojfroyi was becoming active when nectar availability was at its peak for the night and might have been arriving earlier to maintain territories possessing this limited resource. Despite the fact that hummingbirds frequently visited the Majaguillo flowers during the day, A. geoffroyi is likely an important pollinator of this and many other tree species, especially those that bloom only at night. Further research is needed to determine the role this species plays in pollinating highland tree and shrub species, especially in the dry season when diversity and abundance of flowers suitable for bats may be greatest (Bonaccorso

1979). A. geoffroyi was caught significantly more in secondary cloud forest habitat and at the canopy level, both of which suggest its important function as pollinator of pioneer tree species in regeneration areas. While high abundance and permanence in

La Amistad classify A. geojfroyi as one of its keystone species, further studies are needed to quantify the ecological importance of this species as a pollinator in this mountain community.

REPRODUCTIVE ECOLOGY

Most frugivorous bats are thought to be seasonally polyestrous breeders that time their energetically costly reproductive events (e.g., active gestation and lactation) to coincide with peaks in fruit abundance, once during the dry/wet seasonal transition around April or May and again towards the end of the wet season in September and

October (August and Baker 1982, Fleming et al. 1972, Laval and Fitch 1977, 60

Humphrey and Bonaccorso 1979). According to Dinerstein (1986), these reproductive patterns may be associated closely with long-term modal peaks in fruit availability due to variation in rainfall between years.

Presence of lactating females of S. hondurensis and S. morda:x in La Amistad at the beginning and again towards the end of the wet season, suggests that reproductive timing by these sympatric species may be bimodal in nature and driven by the abundance of local fruiting resources. Due to a lack of information on the distribution and abundance of highland bat fruits in La Amistad and an incomplete yearly account of reproductive activity in resident frugivore species (dry season data is missing), this is only a speculation until a more complete data set is available and can be analyzed. Significantly greater numbers of females of S. hondurensis at the beginning of the wet season suggest they may be increasing feeding activity at times of high food abundance to satisfy elevated energetic costs associated with lactation.

A non-significant tendency for a female-biased capture record in June and July also was observed in S. mordax. The greater number of subadults of S. hondurensis and S. morda:x observed in the study area during the middle of the wet season (July-August) suggests that young from the first birth peak (around April or May) became volant at a time of relatively high fruit abundance and then appeared to leave the area around

October, possibly in response to a local depletion of food resources. Minimum reproductive activity was observed for adult females of both species beginning in

October, which further suggests that food resources may become reduced at this time.

Similarly timed reductions in reproductive activity were observed in females of S. hondurensis in the cloud forests of Monteverde (LaVal and Fitch 1977). The fact that 61

·both reproductively active females and subadults of S. hondurensis and S. mordax

were present throughout the wet season suggests that these species may also occur in

the dry season, and hence be permanent or year-round residents of the cloud forests of

LaAmistad.

Like Sturnira, Artibeus species demonstrate a bimodal pattern of reproductive

activity linked to fruit abundance (Fleming et al. 1972, LaVal and Fitch 1977,

Bonaccorso 1979, Dinerstein 1986). However, unlike S. hondurensis and S. mordax,

few reproductively active females and subadults were observed for frugivore species

A. aztecus and A. toltecus. The lack of pregnant or lactating females suggests that

females move from this area before pregnancy is detectable by external palpation,

while the low number of subadults indicates that these females are giving birth

· elsewhere (Stoner 2001). While A. aztecus was captured throughout the wet season,

only adult males and a few non-reproductive females were observed during the first

three months of the study. Beginning in September, both adult males and non­

reproductive adult females began to increase substantially in the community.

Likewise, A. to/tecus was uncommon in La Amistad until September, at which time

capture rate increased, particularly for non-reproductive adult females. The virtual

absence of detectably pregnant and lactating females of A. aztecus and A. toltecus

suggests that these species may only be temporary residents of La Amistad, moving

from other regions or elevations to take advantage of temporarily available food

resources. Or perhaps these species migrate from La Amistad to other areas that

contain more preferred resources, such as Ficus species, to fuel their energetically

demanding reproductive episodes and return to the cloud forests of La Amistad to 62 reside during months of reproductive inactivity. Monitoring during the dry season is necessary to determine the permanence of these species in the La Amistad bat community.

In the nectarivore Anoura geoffeoyi, pregnant females were observed from

August to October in La Amistad. The large number of Majaguillo (Heliocarpus popayanensis) flowers observed in the study area during these months and high degree of pollen loading on captured individuals suggest that abundance of these flowers may trigger A. geoffeoyi to initiate breeding activities. The dry season is considered to be the principal flowering season in Central America (Janzen 1967).

Hence, a constant food supply would be expected to be available to nectarivores in La

Amistad at that time, serving to fuel their reproductive activities. In Brazil, two synchronously flowering plant species have been linked to increases in the number of lactating females and subsequently newly volant young (Baumgarten and Vieira

1994). Abundant protein-rich pollen sources would allow adult females to meet their increased energy demands associated with milk production, while helping newly volant juvenile bats to grow, thereby improving their survival. Previous species accounts in Brazil and Costa Rica also found A. geoffeoyi to be seasonally monoestrous, with adult females giving birth once at the start of the dry season

(Baumgarten and Vieira 1994, Mares and Wilson 1971). The large number of subadult A. geoffeoyi observed in both August and September suggests that young of the year (from the annual birth peak expected in December and January) may not be able to reproduce till their second year, but return to the area to take advantage of an abundant nectar source. 63

The significantly greater number of adult males than females captured in La

Amistad between August and November suggests that males may have become more active to increase their mating encounters with receptive females, as well as augment their energy intake. Furthermore, females of this colonial species undergoing

advanced stages of pregnancy might have been more reluctant to leave the maternity roost, an observation noted by Davis et al. (1968) in females of the insectivorous species Eptesicus fuscus. While A. geoffroyi appears to be a permanent resident of La

Amistad based on its high abundance of reproductive females and subadults, further research during the dry season is needed to determine whether this species remains in the area over the dry season or migrates to dry lowland areas were flowering resources may be more plentiful (Alvarez and Gonzalez 1970). 64

CONCLUSIONS

Despite a relatively recent disturbance ( approximately 13 years ago), the cloud forests of La Amistad have been shown to harbor a diverse chiropteran community.

Due to their numerous ecosystem services, such as seed dispersers, pollinators, and insect regulators, bats facilitate forest regeneration and hence, may be essential for the restoration and maintenance of these cloud forests. Observations of the common bat species during the wet season of 2001 suggest that highland residents display a high degree of flexibility to local conditions. They are capable of dealing with constant low temperatures and of adapting to fluctuations in resource availability both spatially and temporally. Their use of both disturbed and undisturbed cloud forest habitat further demonstrates this plasticity to local disturbance events. By acting as habitat generalists, these mountain residents may satisfy their resource requirements (food and roosts). By partitioning the available resources, these species are able to minimize competition and hence, coexist. They also may maximize their reproductive success by coupling their energetically costly activities of pregnancy and lactation with peaks in food availability.

LIMITATIONS & FUTURE DIRECTIONS

This thesis provides valuable baseline information on the composition and structure of the La Amistad bat community at one point in ecological time, the wet season of 2001. Long-term monitoring is necessary to identify general population trends and determine how seasonal changes in food availability and other factors affect the composition of this highland community and how its members organize 65 themselves with respect to each other and the available resources to mmuruze interspecific competition and coexist.

While temporal trends in abundance of the common phyllostomid species appeared to be in response to changes in food availability, site-specific information on feeding habits of these species, via fecal analysis, and the phenologies of fruiting and flowering plants in La Amistad is needed. By identifying those plant species most important to each of the resident species, more can be inferred about the mechanisms by which intraguild members partition the available food resources to reduce competition. More specifically, how sympatric species S. hondurensis and S. mordax coexist despite similar feeding and roosting requirements. These studies may also serve to identify important alternative food sources for these species at different times of the year (e.g., a frugivore eating pollen during the dry season when fruit abundance is low) and overall, the degree to which phyllostomid bats, as seed dispersers and pollinators, are responsible for cloud forest regeneration in La Amistad.

Future studies might consider the feasibility of employing other sampling protocols, such as acoustic monitoring and roost searches, in conjunction with mist net surveys, which may provide other valuable information on the diversity and ecology of La Amistad bats. Acoustic monitoring is essential for identifying high:. flying insectivorous species, adept at avoiding mist nets. Additional avenues for research may be to explore the role these highland insectivores play in reducing agricultural pests, especially in the agricultural matrix surrounding the park, where pesticide use goes unregulated. Information from roost surveys is important for identifying the roosting requirements of highland species. Little is known as to the 66 degree to which roosts are a limiting resource m highland areas, preventing colonization by species with specific roosting needs.

MANAGEMENT IMPLICATIONS

Bats, especially frugivores, are abundant and important members of the cloud forest community in La Amistad. Their reliance on the fruits of pioneer plant species, matched by their ability to widely disperse these seeds, suggests that these species promote forest regeneration both in secondary-growth habitat and in natural tree gaps occurring in mature cloud forest. By tracking their abundances over time, bats might serve as indicators of the degree of disturbance occurring in a particular habitat and provide valuable information on how local disturbance events, whether natural or human-induced, might affect the resident fauna and flora of La Amistad.

La Amistad cloud forest was important habitat for three endemic frugivore species, which deserve conservation attention based on their limited distributions.

These species, A. aztecus, A. toltecus, and S. mordax, exist only at middle to high elevation forests in Central America, while S. mordax is further restricted to only

Panama and Costa Rica. Furthermore, Parque Internacional La Amistad may be an important temporary home for numerous low and middle elevation species seeking additional food sources. Lichonycteris obscura is a rare species (locally uncommon with a restricted range), most frequently observed at lower elevations and was observed three times in La Amistad during the wet season of 2001. Information on its dietary habits and roosting requirements in La Amistad may help improve conservation of this species throughout its range. 67

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APPENDICES 76

Appendix 1. Mean maximum and minimum temperatures (°C) and total rainfall (mm) registered in Las Nubes ranger station in Parque Internacional La Amistad, Panama, from January to December of 2001.

Month Mean Min Mean Max Total Teme {°C) Teme {°C) Rainfall (mm) Jan 8.4 19 260.4 Feb 8.3 19.9 178.7* Mar 9.5 23.8 57* Apr 10.2 23.1 278.1 May 11.6 23.3 244.5 Jun 11.6 21.9 492.5 Jul 11.3 21.4 330.5 Aug 12.6 22.1 324.1 Sep 11.2 21.8 420.7 Oct 11.8 21.6 316 Nov 12.3 20.4 446.3 Dec 11.3 19.4 516.4

Total 10.8 21.5 3865.2 * Dry season months 77

Appendix 2. Monthly Shannon-Wiener diversity indices (H'), species richness and abundance values for the cloud forests of Parque Internacional La Amistad, Panama, from June to November 2001.

Month H' Spp Richness # Individuals

June 1.63 9 91

July 1.12 9 161

August 1.36 9 157

September 1.15 9 158

October 1.39 9 306

November 1.12 7 177

Total 1.58 15 1050 78

Appendix 3. Presence/absence (+/ -) of bat species in the cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001.

Species Jun Jul Aug Sep Oct Nov No. Months Present A. geoffroyi + + + + + + 6 S. hondurensis + + + + + + 6 A. aztecus + + +. + + + 6 S. mordax + + + + + + 6 A. toltecus + + + + + 5 M keaysi + + .+ + + 5 . M oxyotus + + + 3 M microtis + + + 3 E. hartii + + + 3 G. soricina + + 2 P. vittatus + + 2 L. obscura + + 2 A. lituratus + 1 E. brasiliensis + 1 M nigricans + 1

Total SJ!J! 9 9 9 9 9 7 79

Appendix 4. Monthly diversity indices and species richness values for primary and secondary cloud forest in Parque Internacional La Arnistad, Panama, from June to November 2001.

Shannon-Wiener Diversity Index, H' (Species Richness, R) Month Primary forest Secondary Forest June 1.32 (7) 1.57 (8) July 1.69 (8) 0.60 (5) August 1.59 (6) 1.21 (7) September 1.22 (5) 1.02 (8) October 1.32 (6) 1.28 (8) November 0.74 (6) 1.26 (6)

Mean H' (Total R) 1.31 (12) 1.16 (13) 80

Appendix 5. Presence of bat species in the primary (P) and secondary (S) cloud forests of La Amistad from June to November 2001.

Species Jun Jul Aug Sep Oct Nov No. Months Present A. geoffroyi * P,S P,S P, S P, S P,S P,S 6, 6 S. hondurensis * P,S P,S P, S P, S P,S P,S 6, 6 A. aztecus* P,S P,S P,S P,S P,S P,S 6, 6 S. mordax* P,S P,S P,S P,S P,S P,S 6, 6 A. toltecus* p s s P,S P,S 3,4 M keaysi s s s s s o, 5 M oxyotus* p p s 2, 1 M microtis p p p 3,0 E. hartii* p p s 2, 1 G. soricina * s p 1, 1 P. vittatus s s o, 2 A. lituratus s o, 1 L. obscura* P,S s 1,2 E. brasiliensis p 1, 0 M nigricans * P,S 1, 1

Total SJ;!J;! 7, 8 8, 5 6, 7 5, 8 6, 8 6, 6 * Found in both forest types 81

Appendix 6. Vertical stratification by most common bat species in primary and secondary cloud forests of Parque Internacional La Amistad, Panama, from June to November 2001.

PRIMARY FOREST SECONDARY FOREST Sf!ecies Canol!r Understory Total Canol!r Understory Total A. geoffroyi 81** 9 90 259** 49 308 A. aztecus 123** 13 136 128** 10 138 S. hondurensis 49** 11 60 164** 98 262 S. mordax 22 14 36 23 29 52 A. toltecus 11** 0 11 33** 4 37 M keaysi 0 0 0 3 11 * 14

TOTAL 286 47 333 610 201 811 * Significantly different at p < 0.05. ** Significantly different at p < 0.001. 82

Appendix 7. Mean weights (g) and mean forearm lengths (mm) by sex for bat species captured in cloud forests of Parque Internacional La Amistad, Panama, between June and November 2001.

Adult Indiv. Mean Mass ± St. Dev. Mean Forearm ± St. Dev. S~ecies #M:#F Ad Males Ad Females Ad Males Ad Females A. geoffroyi 202: 113 15.6 ± 1.3 15.5 ± 1.5 42.5 ± 1.1 42.9 ±1.3 S. hondurensis 68: 129 23.1 ± 2.2 20.8 ± 2.0 44.4 ± 1.2 43.9 ± 1.2 A. aztecus 135: 132 24.5 ± 2.1 25.1 ± 1.9 47.7 ± 1.5 48.2 ± 1.7 S. mordax 28: 51 29.1± 3.2 26.5 ± 2.8 47.3 ± 2.1 46.5 ±2.0 A. toltecus 9: 36 15.3 ± 0.9 16.5 ± 1.9 40.3 ± 1.2 41.6 ± 1.6 M keaysi 1: 6 5±0 5.8 ± 1.3 37±0 36.3 ± 1.9 . M oxyotus 0:2 8±0 41 ±0 M microtis 1 : 1 9±0 9±0 35 ±0 35 ±0 E. hartii 2:3 20 ± 1.4 19 ± 2.6 40.5 ± 0.7 36.3 ± 0.7 G. soricina 1 : 1 7±0 12 ±0 34± 0 39±0 P. vittatus 2:0 56.5 ± 0.7 59.5 ± 0.7 A. lituratus 1 : 1 69±0 74±0 69±0 69±0 L. obscura 1 : 0 7±0 31 ± 0 E. brasi/iensis 0:0 M nigricans 3:1 5 ± 1 5±0 36.7 ± 0.6 37±0 Appendix 8. Reproductive condition for adult females of highland bat species caught in Parque Internacional La Amistad, Panama, between June and November of 2001. Abbreviations are: NR, Non-reproductive; P, Pregnant; L, Lactating.

Species Total Adult JUN JUL AUG SEP OCT NOV Females Anoura geoffroyi 109 lONR/ lL llNR 16NR/ lP llNR/ 13P 31NR/ 14P lNR Sturnira hondurensis 128 6NR/ 13L 25NR/ 17L 9NR SNR/ 3L 35NR/ lP / 3L llNR Artibeus aztecus 130 lNR lNR SNR l0NR 42NR 71NR Sturnira mordax 48 3NR/ SL 3NR/ 12L lNR/ lP / lL 2NR/ 3L 8NR SNR/ lL Artibeus toltecus 36 6NR/ lP / 2L 27NR Myotis keaysi 6 1NR/2L lNR lNR lNR Myotis oxyotus 2 lNR lNR Echisthenes hartii 3 lNR lNR lNR Myotis nigricans 1 lNR 00 Micronycteris microtis 1 INR w Glossophaga soricina 1 INR Artibeus lituratus 1 lNR