Island Bats: Evolution, Ecology, and Conservation

I s l a n d B a t s

I s l a n d B a t s

Evolution, Ecology, and Conservation

Edited by

Theodore H. Fleming and Paul A. Racey

The University of Chicago Press

Chicago and London

Theodore H. Fleming is professor emeritus of biology at the

University of Miami in Coral Gables, Florida.

Paul A. Racey is the Regius Professor of Natural History (emeritus) in the

School of Biological Sciences at the University of Aberdeen, Scotland.

The University of Chicago Press, Chicago 60637

The University of Chicago Press, Ltd., London

© 2009 by The University of Chicago

All rights reserved. Published 2009

Printed in the United States of America

18 17 16 15 14 13 12 11 10 09 1 2 3 4 5

ISBN-13: 978-0-226-25330-5 (cloth)

ISBN-10: 0-226-25330-9 (cloth)

Library of Congress Cataloging-in-Publication Data

Island bats: evolution, ecology, and conservation / edited by Theodore H. Fleming

and Paul A. Racey.

p. cm.

Includes index.

ISBN-13: 978-0-226-25330-5 (cloth : alk. paper)

ISBN-10: 0-226-25330-9 (cloth: alk. paper) 1. Bats. 2. Bats—Ecology.

3. Bats—Conservation. 4. Bats—Islands of the Pacific. 5. Bats—West Indies.

6. Island Animals­ I. Fleming, Theodore H. II. Racey, P. A.

QL737.C5185 2009

599.4’1752­—dc22

2009028840

a The paper used in this publication meets the minimum requirements of the

American National Standard for Information Sciences—Permanence of Paper for

Printed Library Materials, ANSI Z39.48-1992.

C O NT E NTS

1 An Introduction to Island Bats

Theodore H. Fleming and Paul A. Racey 1

P A R T 1 . E V O L U T I O N O F I SLAND B ATS

2 New Perspectives on the Long-Term Biogeographic Dynamics and

Conservation of Philippine Fruit Bats

Lawrence R. Heaney and Trina E. Roberts 17

3 Crossing the Line: The Impact of Contemporary and Historical Sea

Barriers on the Population Structure of Bats in Southern Wallacea

Lincoln H. Schmitt, Susan Hisheh, Agustinus Suyanto, Maharadatunkamsi,

Christopher N. Newbound, Darrell J. Kitchener, and Richard A. How 59

4 Earth History and the Evolution of Caribbean Bats

Liliana M. Dávalos 96

5 Phylogeography and Genetic Structure of Three Evolutionary

Lineages of West Indian Phyllostomid Bats

Theodore H. Fleming, Kevin L. Murray, and Bryan Carstens 116

P A R T 2 . E C O L O G Y O F I SLAND B ATS

6 Physiological Adaptation of Bats and Birds to Island Life

Brian K. McNab 153

7 The Role of Pteropodid Bats in Reestablishing Tropical Forests

on Krakatau

Louise A. Shilton and Robert J. Whittaker 176

8 Macroecology of Caribbean Bats: Effects of Area, Elevation, Latitude, and

Hurricane-Induced Disturbance

Michael R. Willig, Steven J. Presley, Christopher P. Bloch, and Hugh H. Genoways 216

9 Bat Assemblages in the West Indies: The Role of Caves

Armando Rodríguez-Durán 265

v

10 Island in the Storm: Disturbance Ecology of Plant-Visiting Bats on the

Hurricane-Prone Island of Puerto Rico

Michael R. Gannon and Michael R. Willig 281

11 Bats of Montserrat: Population Fluctuation and Response to Hurricanes

and Volcanoes, 1978–2005

Scott C. Pedersen, Gary G. Kwiecinski, Peter A. Larsen, Mathew N. Morton, Rick A.

Adams, Hugh H. Genoways, and Vicki J. Swier 302

12 Flying Fox Consumption and Human Neurodegenerative Disease

in Guam

Sandra Anne Banack, Paul Alan Cox, and Susan J. Murch 341

P A R T 3 . C O NS E R V AT I O N O F I SLAND B ATS

13 The Ecology and Conservation of Malagasy Bats

Paul A. Racey, Steven M. Goodman, and Richard K. B. Jenkins 369

14 Conservation Threats to Bats in the Tropical Pacific Islands and Insular

Southeast Asia

Gary J. Wiles and Anne P. Brooke 405

15 The Ecology and Conservation of New Zealand Bats

Colin F. J. O’Donnell 460

16 Global Overview of the Conservation of Island Bats: Importance,

Challenges, and Opportunities

Kate E. Jones, Simon P. Mickleburgh, Wes Sechrest, and Allyson L. Walsh 496

List of Contributors 531

Subject Index 535

Species Index 539

Color gallery follows page 314

vi Contents



C h a p t e r 1

An Introduction to Island Bats

Theodore H. Fleming and Paul A. Racey

Introduction

One of us (THF) recently polled colleagues in his department about their im￾mediate visual response to the phrase “tropical islands.” In addition to the

usual images of aquamarine seas, turquoise lagoons, white sandy beaches,

and lush green vegetation, people mentioned coral reefs, volcanoes, basalt,

palm trees, and hammocks. By and large most of these respondents pictured

benign scenes of tranquility and beauty—scenes that you would typically see

in tourist brochures. But, as will become abundantly clear in this volume, the

biological reality of island life is far from benign and tranquil. Ask these same

people to describe “tropical islands” in less visual and more biological terms,

and their responses might include such terms as “limited species diversity,”

“limited space and resources,” “fewer predators,” “physiologically harsh en￾vironments,” “frequent disturbances caused by tropical storms, earthquakes,

and erupting volcanoes,” and, with increasing frequency and intensity, “hu￾man disturbance.” For the organisms that have successfully colonized them,

isolated oceanic islands worldwide can be anything but benign and Eden-like

places to live.

Despite, or perhaps because of, their isolation, and limited space, resources,

and species richness, islands and their species have long fascinated biologists.

With their reputation as being living laboratories, islands have provided ecolo￾gists and evolutionary biologists with a much greater number of fundamen￾tal concepts than their total area (about 3% of Earth’s surface; Whittaker

1998) might suggest. Beginning with Darwin’s and Wallace’s seminal idea of

organic evolution via natural selection (Darwin and Wallace 1858), these con￾cepts include adaptive radiation, Sewall Wright’s (1931) island and stepping

stone models of population genetics, Ernst Mayr’s (1942) concept of allopatric

speciation and the importance of founder effects, Edward O. Wilson’s (1961)

taxon cycle, Robert MacArthur and E. O. Wilson’s (1963, 1967) equilibrium

theory of island biogeography and r and K selection, Jared Diamond’s (1975)

community assembly rules, Graeme Caughley’s (1994) small-population para￾digm in conservation biology, and Ilka Hanski and Michael Gilpin’s (1997)

recent versions of metapopulation theory (table 1.1). Collectively, these concepts

T. H. Fleming and P. A. Racey

represent many of the basic cornerstones of modern evolutionary, ecological,

and conservation thinking.

In addition to inspiring many important biological concepts, islands and

their faunas and floras have been endlessly fascinating to biologists because

of their intrinsic physical and biological features, many of which are summa￾rized in table 1.2. The important physical features associated with islands are

generally well-known. Two of those features—geological substrates and degree

of natural disturbance—are particularly important for bats, the major subject

of this book. Like their continental relatives, many island-dwelling bats use

caves for their day roosts, and basic island geology can determine the extent

and physical nature of caves. Many islands lie on the boundaries of crustal

plates or above crustal “hot spots” and hence occur in areas of intense seismic

activity. This activity can have strong negative effects on island floras and fau￾nas. Additionally, many tropical islands occur in hurricane or typhoon zones,

whose storms can also have devastating effects on populations of plants and

animals.

Biological features of islands include reduced species richness (impover￾ishment) and taxonomically and ecologically skewed (disharmonic) faunas

and floras favoring organisms with excellent over-water dispersal abilities

(table 1.2). Interesting ecological features of island endemics often include

Table 1.1. Major concepts or theories in evolution and ecology resulting from or inspired by

islands and their biogeography (modified from Whittaker 1998).

Concept or Theory Authors and/or examples

Evolution by natural selection C. Darwin (Galapagos), A. Wallace (Indonesia)

Adaptive radiation Galapagos finches, Hawaiian honeycreepers, Hawaiian

Drosophila, New Guinea birds of paradise, Caribbean Anolis,

Madagascan lemurs and tenrecs, Galapagos Scalesia, Hawaiian

silverswords

Island and stepping stone

models of population genetics

S. Wright

Allopatric speciation and

founder effects

E. Mayr (New Guinea, Pacific islands)

Taxon cycle E. Wilson (ants, Melanesia), R. Ricklefs (birds, Lesser Antilles)

Equilibrium theory of island

biogeography

R. MacArthur, E. Wilson (Pacific and Caribbean islands)

r and K selection R. MacArthur, E. Wilson

Community assembly rules J. Diamond (birds, New Guinea and surrounding islands)

Small-population paradigm

in conservation biology

G. Caughley (small island populations)

Metapopulations R. Levins, I. Hanski, M. Gilpin

An Introduction to Island Bats

reduced fecundity and dispersal ability (e.g., loss of flight), higher popula￾tion densities, broader ecological niches, reduced fear of predators, larger or

smaller body sizes, and elevated rates of extinction compared with their con￾tinental relatives. Island faunas and floras are also notable for harboring high

proportions of endemic species such that islands contribute (or contributed)

a disproportionately high number of species to Earth’s biodiversity. Levels of

endemism are uniformly high in flowering plants, birds, and bats on islands. In

terms of numbers of endemic families or subfamilies and their genera and spe￾cies, island birds are more diverse than island bats (tables 1.3 and 1.4). Fourteen

families or subfamilies of birds containing 47 genera and 86 species are island

endemics, compared with only 5 families or subfamilies of bats containing 7

genera and 25 species. With 5 endemic families, Madagascar has the greatest

number of endemic bird families. With 2 endemic subfamilies of phyllostomid

bats, the West Indies is the site of greatest endemism at higher taxonomic levels

in bats. Two other groups of West Indian bats—family Natalidae and the phyl￾lostomid tribe Stenodermatina of subfamily Stenodermatinae—evolved in the

Caribbean and then colonized the mainland of Mexico and Central and South

America (Dávalos, chapter 4, this volume) and hence are not strictly endemic

to those islands.

Finally, island faunas and floras are notable because of their high conserva￾tion concerns. About one-quarter of the 25 global biodiversity hot spots identi￾fied by Myers et al. (2000) because of their exceptional conservation concern, for

example, are island systems. These areas include the Caribbean, Madagascar,

Sundaland, Wallacea, the Philippines, Polynesia/Micronesia, and New Zea￾land. Each of these areas contains endemic species of island-dwelling bats,

Table 1.2. What’s so special or interesting about islands?

Topic Details

Physical features Size, number or habitats, geological substrates, isolation, disturbance

prone (nonanthropogenic)

Biological features Impoverishment, disharmony, dispersal, loss of dispersal ability,

reproductive changes, body-size changes, broad ecological niches,

high population density, tameness, extinction prone

Biodiversity features Disproportionately high number of species overall occur on islands.

Plants: about 1/6 of all species occur on islands; birds: about 1/6 of

all species occur on islands; bats: 3/17 families occur only on islands;

reptiles: 1/2 of all species of Anolis lizards occur on islands

Conservation concerns Disproportionately high number of extinctions occur on islands. Birds:

40× higher extinction rate in island species than continental species;

mammals: except for bats (~14%), 83–100% of West Indian land mam￾mals are extinct; reptiles: “majority of extinctions have occurred on

islands”

Sources: Based on Grant 1998; Whittaker 1998; Williamson 1981.

Table 1.3. Extant endemic families and subfamilies of island birds

Order or suborder Family or subfamily Name Island N genera N species

Dinornithoiformes Apterygidae Kiwis N Zealand 1 3

Gruiformes Rhynochetidae Kagu N Caledonia 1 1

Gruiformes Mesitornithidae Mesites Madagascar 2 3

Coraciiformes Todidae Todies W Indies 1 5

Coraciiformes Brachypteraciidae Ground rollers Madagascar 4 5

Coraciiformes Leptosomatidae Cuckoo rollers Madagascar 1 1

Tyranni Acanthisittidae N Z wrens N Zealand 2 4

Tyranni Philepittidae Asities Madagascar 2 4

Passeres Callaeidae Wattlebirds N Zealand 3 3

Passeres Vangidae Vangas Madagascar 15 22

Passeres Dulidae Palmchat W Indies 1 1

Passeres Rhabdornithidae Philippine creepers Philippines 1 2

Passeres Drepanidinae Hawaiian honeycreepers Hawaii 10 23

Passeres Emberizidae, Geospizinae Galápagos finches Galápagos 3 13

Total 14 47 90

Sources: Gill 1990; Craycraft et al. 2003.

An Introduction to Island Bats

many of which are considered to be “threatened” by the IUCN. More generally,

extinction rates of island plants and animals are considerably higher than those

of their continental relatives. In birds, for example, extinction rates on islands

are 40 times higher than they are elsewhere in the world. Similarly, in the West

Indies, 83–100% of nonvolant mammals, depending on family, are extinct, al￾though only 14% of West Indian bats are known to be extinct. Likewise, most

known extinctions of reptiles have occurred on islands. Most, but not all (e.g.,

West Indian bats; Morgan 2001), of these extinctions have an anthropogenic

cause resulting from habitat destruction, overhunting, and the introduction of

exotic species (including pathogens).

Overview of Bats on Islands

Because they can fly, bats often represent most or all of the extant mammals on

isolated oceanic islands. They are the only native land mammals on Hawaii,

New Zealand, and many Pacific islands, for example. Island bats also contrib￾ute significantly to the overall species richness of bats. Jones et al. (chapter 16,

this volume) report that fully 60% of all bat species live on islands (n = 925)

and that 25% of all bats are island endemics; 8% of all bats are single-island

endemic species. Thus islands have played an especially important role in the

overall evolution of bats. In addition to being of considerable evolutionary

interest, plant-visiting bats are particularly important as pollinators and seed

dispersers in tropical island ecosystems (e.g., Cox et al. 1991; Cox et al. 1992;

Elmqvist et al. 1992; Rainey et al. 1995). Banack’s work (1998) in American

Samoa, for example, indicates that two species of Pteropus flying foxes feed on

flower and fruit resources of 78 plant species throughout their ranges and on

Table 1.4. Extant endemic families and subfamilies of island bats

Family or subfamily Name Islands N genera N species

Pteropodidae,

Nyctimeninae

Tube-nosed bats New Guinea,

Philippines

(and Australia)

2 15

Myzopodidae Old World

sucker-footed bats

Madagascar 1 2

Mystacinidae New Zealand

short-tailed bats

New Zealand 1 2

Phyllostomidae,

Phyllonycterinae

West Indian

flower bats

Greater Antilles 2 5

Phyllostomidae,

Brachyphyllinae

West Indian

fruit bats

Greater and

Lesser Antilles

1 2

Total 5 7 26

Source: Simmons 2005.

T. H. Fleming and P. A. Racey

69 plant species on Samoa alone. Many of their food resources are produced

by canopy trees in primary forests, and bats are likely to be their sole dispers￾ers. Although fruit-eating bats appear to play a more important role in the

early stages of ecological succession in the Neotropics than in the Paleotropics

(Muscarella and Fleming 2007), pteropodid bats have played an important role

in the recolonization of Krakatau by plants (e.g., Whittaker and Jones 1994).

The ability to retain seeds in viable condition in their guts for up to 19 hours

makes pteropodid bats especially important as long-distance dispersers of the

seeds of island plants (Shilton et al. 1999). Finally, island bats are the source

of considerable conservation concern. Jones et al. (chapter 16, this volume)

indicate that nearly 50% of threatened bats worldwide (i.e., species designated

as VU, EN, or CR in IUCN 2006) are island endemics; an additional 22% of

threatened bats are single-island endemics. Not only will the loss of these bats

contribute to a decrease in global biodiversity, but it also represents the loss of

important ecological services such as predation on insects as well as pollination

and seed dispersal. McConkey and Drake (2006), for instance, reported that

seed dispersal by flying foxes declined nonlinearly with a decline in relative

bat abundance on Vava’u (Tonga, Polynesia). Below a threshold abundance

value, bats moved <1% of the seeds they handled <5 m from the canopies of

fruit trees, whereas above this threshold they removed up to 58% of the seeds

>5 m. From these results, McConkey and Drake (2006) concluded that flying

foxes can become functionally extinct well before their actual numbers decline

to zero. In summary, island bats and their fate are of considerable interest for

many evolutionary, ecological, and conservation reasons.

Scope of This Book

This book is the outgrowth of a symposium on island bats held at the 2004

annual meeting of the Association for Tropical Biology and Conservation in

Miami, Florida. Twelve of the thirteen papers delivered at that symposium

appear as chapters in this book. After the meeting, we invited three additional

colleagues or groups of colleagues to contribute chapters to this book, which

is divided into three major sections.

Part 1 deals with the evolution of island bats and contains four chapters.

Two chapters discuss bats in the Wallacean region of Indonesia and the Philip￾pines and two discuss bats in the West Indies. One common theme that runs

through these chapters is the effect that changes in sea level has had on connec￾tions between island and mainland populations and among island populations.

In both the Philippines and Wallacea, islands that are currently separated by

shallow water channels formed larger islands in the Pleistocene, and bats that

live on the same Pleistocene islands tend to be more closely related than bats

that lived on other Pleistocene islands. Deepwater channels that persisted dur￾ing the Pleistocene have also had a strong effect on the genetic structure of bats

An Introduction to Island Bats

in the Philippines, Wallacea, and the Greater Antilles. Dávalos’s analysis of

phylogenetic relationships within seven West Indian bat lineages in three fami￾lies reveals the strong imprint of geological history on bat relationships. Three

periods of low water during the Miocene (between 16 and 5 Ma) promoted

colonization of northern Caribbean islands by several lineages of bats and

helped shape patterns of divergence within these lineages. A second common

theme is that, contrary to theoretical expectations, populations of many island

bats do not contain lower amounts of genetic variation than mainland popula￾tions and that even on small, isolated islands, bat populations tend to contain

substantial genetic variation. Historically, island bat populations have often

been large and resistant to abiotic disturbances such as hurricanes, typhoons,

and volcanic eruptions. Rather than being extinction-prone, as postulated by

the MacArthur-Wilson equilibrium theory of island diversity, island bats have

actually been extinction-resistant (prior to the arrival of humans).

Several notable findings emerge from these four chapters. First, Heaney and

Roberts used both allozymes and mitochondrial DNA (mtDNA) to estimate

rates of between-island gene flow in six species of Philippine pteropodid bats.

While the two data sets generally give congruent results, these authors note

that allozymes reflect gene flow over much longer periods of time than does

mtDNA. This is because mutations in allozyme loci don’t often create new

alleles, whereas nucleotide mutations in DNA are immediately visible. As a

result, estimates of genetic subdivision will be higher and rates of gene flow

lower when they are measured using mtDNA than when they are measured

using allozymes. Second, Schmitt et al. point out that, contrary to the common

view that Wallacea is merely a transition zone between the floras and faunas of

Asia and Australasia, it is an evolutionarily dynamic region on its own right.

Their studies show that these islands have produced a number of endemic spe￾cies of bats as well as other mammals and reptiles. Third, Dávalos’s analysis of

West Indian bats helps to dispel the common belief that colonization of islands

from mainlands is a one-way street. Her analyses show that three to six lin￾eages of bats that are currently distributed from northern Mexico to Paraguay

may trace their ancestry to the West Indies. Island groups that have success￾fully colonized (and radiated in some cases) the Neotropical mainland include

mormoopid, natalid, and phyllostomid bats representing a variety of trophic

adaptations. Finally, Fleming et al.’s analysis of three West Indian lineages of

phyllostomid bats indicates that island-mainland gene exchange is still occur￾ring in Artibeus jamaicensis; that, contrary to general expectations, two “old

island endemics” (Erophylla sezekorni and E. bombifrons) show no evidence of

low genetic diversity or high levels of between-island subdivision; and that the

species Macrotus waterhousii, whose geographic distribution includes Mexico

and the Greater Antilles, actually consists of a series of endemic island species

that have been isolated from the mainland and each other for substantial peri￾ods of time. Differences in the degree of genetic subdivision within the latter

T. H. Fleming and P. A. Racey

two taxa are striking and point to the importance of ecological lifestyle (E.

sezekorni and E. bombifrons are feeding generalists; M. waterhousii is a specialist

on large insects) and trophic position, rather than length of island residency

per se, in determining the genetic structure of island bats.

Part 2 deals with the ecology of island bats and contains seven chapters.

Topics included in this section range from the physiological challenges that

island bats face to the effects of major abiotic disturbances (hurricanes and vol￾canoes) on bat populations. Included here is a fascinating discussion of a four￾trophic-level interaction among humans, fruit-eating bats, their food plants,

and symbiotic cyanobacteria that has important health implications. In his

review of the metabolic and life-history characteristics of island bats and birds,

McNab points out that energy reduction and a lower cost of living are common

themes. Smaller size, lower basal metabolic rates, reduced fecundity, and, in at

least 11 families of birds, the evolution of flightlessness are the major ways by

which island endotherms have reduced their costs of living in resource-limited

environments. Unlike birds, island bats have not evolved flightlessness, but

the New Zealand endemic short-tailed bats (Mystacina) spend considerable

amounts of time foraging on and under forest litter for insects. McNab points

out that many of the metabolic and life-history adaptations found in island

bats and birds have made them highly vulnerable to humans and the exotic

predators they have brought to islands.

Shilton and Whittaker provide the first detailed account of the role of ptero￾podid bats as seed dispersers in the Krakatau island system. Their data indicate

that these bats have played an important role in the revegetation of these four

volcanic islands for over a century. Although bats of the genus Cynopterus—the

most common pteropodids in this system—are generally sedentary foragers,

they sometimes fly between islands and move seeds from one island to an￾other. Strong-flying Pteropus vampyrus bats occasionally visit the islands from

Sumatra and Java and are also important long-distance seed dispersers. They

conclude that the role of bats as long-distance seed dispersers and as agents of

revegetation of Krakatau has been underestimated.

Four papers in this part deal with the ecology and macroecology of West

Indian bats. Willig et al. use a battery of multivariate analyses to determine the

relative importance of latitude, island area, elevation, degree of isolation, and

hurricane-caused disturbance for determining an island’s bat species richness

and guild structure. They divide Caribbean islands into three major groups—

Greater Antilles, Lesser Antilles, and Bahamas—to conduct their analyses. Of

the five independent variables, island area (along with island elevation in the

Greater and Lesser Antilles) is the strongest predictor of bat diversity in each

island group separately and in all 64 islands collectively. Hurricane disturbance

and interisland distances are not significant predictors of bat diversity, which

implies that any losses of species caused by strong storms are quickly recouped

via interisland dispersal. These results reinforce the idea that island bats are in-